Mineral weathering in ectomycorrhizosphere of subalpine fir (Abies lasiocarpa (Hook.) Nutt.) as revealed by soil solution composition

Forest Ecology and Management 133 (2000) 61±70

Mineral weathering in ectomycorrhizosphere of subalpine ®r (Abies lasiocarpa (Hook.) Nutt.) as revealed by soil solution composition J.M. Arocena*, K.R. Glowa Forestry Program, Faculty of Natural Resources and Environmental Studies, University of Northern British Columbia, 3333 University Way, Prince George, BC, V2N 4Z9, Canada Accepted 6 October 1999

Abstract The soil solution is considered an important index of nutrient availability, because it mimics the ®eld conditions when plant roots obtained their nutrition, and re¯ects the weatherability of a particular soil mineral. The composition of soil solution is sensitive to physical, biological and chemical changes to soil systems, including the presence of fungal hyphae and rhizomorphs from ectomycorrhizal colonization. The objective of this paper is to compare the soil solution composition extracted from two ectomycorrhizosphere soils (or soil environment in the vicinity of ectomycorrhizae) to nonectomycorrhizosphere soil of subalpine ®r (Abies lasiocarpa (Hook.) Nutt.) in the Ae horizon of Gray Luvisol in northern British Columbia. We extracted the soil solution from ectomycorrhizosphere of Piloderma spp. (ECS-A), Mycelium radicis atrovirens-cottony yellow-brown types (or where Piloderma spp. colonization was <2%) (ECS-B), and from nonectomycorrhizosphere soils (N-ECM). These soils had been equilibrated anaerobically at ®eld capacity for three weeks at room temperature. The content of major cations in solution, regardless of soil sample, followed the order Ca2‡ > K‡ > Mg2‡. We found that the concentrations as well as the activities of these cations followed the order ECS-A > ECS-B > N-ECM. A similar trend is true for K00 , a parameter for the availability of soil K‡. These trends are consistent to the results of geochemical models of more negative saturation index (or enhanced weathering) for muscovite, chlorite, anorthite and K-feldspars in ECSA and ECS-B compared to N-ECM soils. Low pH in the ectomycorrhizosphere sample is believed to be responsible for the differential breakdown of soil minerals and the increased availability of K‡, Ca2‡ and Mg2‡ in soil solution. The results from this study could have practical application in forestry, such as in use of fungal inoculation for improved survival of seedlings, especially in areas that shows de®ciency of potassium and calcium. # 2000 Elsevier Science B.V. All rights reserved. Keywords: Ectomycorrhizosphere soils; Ectomycorrhizae; Saturation index; Soil solution; Piloderma spp.; Mycelium radicis atrovirens (MRA)

1. Introduction

*

Corresponding author. Tel.: ‡1-250-960-5811; fax: ‡1-250-960-5538. E-mail address: [email protected] (J.M. Arocena)

Management of forests for long-term productivity depends on the ability of soil to maintain the supply of essential nutrients from the weathering of soil minerals. Breakdown of soil minerals, such as mica and feldspars, will provide the soil solution with elements

0378-1127/00/$ ± see front matter # 2000 Elsevier Science B.V. All rights reserved. PII: S 0 3 7 8 - 1 1 2 7 ( 9 9 ) 0 0 2 9 8 - 4

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such as K‡, Ca2‡ and Mg2‡ that are essential to plant growth. Soil solution composition is considered as one of the most important indices of absolute bioavailability of nutrients (Wolt, 1994). At any given time, the elemental composition of the soil solution provides a measure of available essential elements, because it mimics the ®eld conditions when plant roots obtained their nutrition. Soil solution composition is the hub predictor of soil processes, such as mineral weathering assuming a steady state condition exists between soil minerals and soil solution, and re¯ects the net weatherability of a suite of minerals. The soil solution represents the natural medium for plant growth and its composition had been used to diagnose plant growth response to the availability of essential nutrients (McColl, 1975; Hendrickson et al., 1989; Zabowski and Ugolini, 1990; Likens et al., 1994). In interpreting the composition of soil solution for plant nutrition, Wolt (1994) suggested the use of activity ratio (e.g. K-intensity), calculated from elemental composition of soil solution, to account for the multitude of soil processes affecting the availability of nutrients for plant uptake. The composition of soil solution is sensitive to physical, biological and chemical changes to soil systems (Wolt, 1994), including the presence of fungal hyphae and rhizomorphs from ectomycorrhizal colonization. Ectomycorrhizal (ECM) associations are established when ectomycorrhizal fungi form an intercellular Hartig net and a sheath of hyphae mantle around the root (Foster et al., 1983). These ubiquitous rootfungal associations modify soil processes such as mineral weathering and nutrient uptake, especially in the ectomycorrhizosphere or the soil environment in the immediate vicinity of the ECM (Sylvia et al., 1998; Jongmans et al., 1997; Paris et al., 1994; Snetselaar et al., 1990; Perry et al., 1987; Rygiewicz and Bledsoe, 1984; Rygiewicz et al., 1984). The weathering rate of micaceous mineral to a 2 : 1 expandable type of clay is faster in rhizosphere compared to nonrhizosphere soils (Hinsinger and Jaillard, 1993; Kodama et al., 1994). Precipitation of minerals such as amorphous oxides of Al, silica, and calcium oxalate occur in the rhizosphere zone (April and Keller, 1990; Cromack et al., 1979). Berthelin (1983) reported that microbial weathering of soil minerals in rhizosphere soils depends on the species of microorganisms. In

terms of nutrient availability, Hinsinger and Jaillard (1993) indicated that K concentration in soil solution from rhizosphere soils is lower than the non-rhizosphere soil. In Sweden, Jongmans et al. (1997) reported that in granitic rocks, direct hyphal connections between Suillus granulatus and Piloderma croceum and the tree roots were indications of direct participation of ECM in tree nutrition. Snetselaar and Whitney (1990) also indicated that the mycorrhizae of Monotropa uni¯ora may regulate the availability of Ca2‡ in plants associated with this angiosperm. Rygiewicz and Bledsoe (1984) and Rygiewicz et al. (1984) indicated that ECM increased uptake of K‡ and NH4‡ ions from soil solution by coniferous trees. In forest soils research, there is a need to understand the role of ECM in soil mineral weathering related to the supply of essential elements for tree nutrition (Courchesne and Gobran, 1997). Among others, one approach to the above problem is to integrate in situ ECM information with the soil solution composition to determine the availability of nutrients from a particular ECM colonization. In this study, we compared the composition of soil solution extracted from ectomycorrhizosphere and non-ectomycorrhizosphere soils of sub-alpine ®r (Abies lasiocarpa (Hook.) Nutt.) in the Ae horizon of a Gray Luvisol to determine the role of ECM in the long-term supply of essential elements, particularly K‡, Ca2‡ and Mg2‡, in soil solution. 2. Materials and methods 2.1. Description of the study area and sample collection The study area was within the sub-boreal forests and located near the campus of the University of Northern British Columbia (UNBC) in Prince George, Canada. The soil was a Brunisolic Gray Luvisol (Dawson, 1989), developed on drumlinized basal till with 4cm thick forest ¯oor layers and 5-cm thick Ae horizon. The dominant minerals in the clay fractions from the Ae horizon are muscovite, 2 : 1 expanding type, chlorite and kaolinite (Arocena et al., 1999). Soil pH and selected properties of the Ae horizon are given in Table 1. Mean annual precipitation ranges from 500 to 800 mm, and mean annual temperature is 3.38C.

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Table 1 Mean (and standard deviation) values for pH, total N, exchangeable Ca, Mg and K, and abundance (%) of major morphotypes of ectomycorrhizae in two ectomycorrhizosphere (ECS-A and ECS-B) and non-ectomycorrhizosphere (N-ECM) soils. (after Arocena et al., 1999) Selected soil properties/ECM morphotypes

ECS-A

ECS-B

N-ECM

Selected soil properties (n ˆ 3) Soil pHa Exchangeable Ca** (cmolc kgÿ1 soil) Exchangeable Mg** (cmolc kgÿ1 soil) Exchangeable K** (cmolc kgÿ1 soil) Dominant clay mineralsb Dominant sand mineralsb

4.6 (0.25) 8.1a (0.37) 1.1a (0.05) 0.32a (0.01) Mi, Ch, 2 : 1 Exp., Kt, Gt Qtz, Ab, An, K-Fd

4.9 (0.26) 5.6b (1.1) 0.74b 0.25b (0.02) Mi, Ch, 2 : 1 Exp., Kt, Gt Qtz, Ab, An, K-Fd

5.2 (0.60) 4.2b (0.37) 0.64b (0.05) 0.15c (0.01) Mi, Ch, 2 : 1 Exp., Kt, Gt Qtz, Ab, An, K-Fd

Ectomycorrhizal morphotypes (n ˆ 6) Piloderma spp. Mycelium radicis atrovirens (MRA) Cottony-cream yellow-brown (CYB) Cenococcum geophilum Fr.

66 (3.3) 2.2 (1.4) 3.5 (5.4) 17 (7)

1.6 (2.3) 32 (28) 24 (21) 17 (13)

± ± ± ±

**

p < 0.01; For each row, means with similar letters are not significantly different. n ˆ 6. b Mi, Mica (muscovite); Ch, chlorite; Exp, 2 : 1 expanding clays (e.g. montmorillonite); Kt, kaolinite; Gt, goethite; Qtz, quartz; Ab, albite; An, anorthite; K-Fd, K-feldspars. a

Vegetation is dominated by hybrid white spruce (Picea glauca  P. engelmannii), subalpine ®r (Abies lasiocarpa), and lodgepole pine (Pinus contorta var. latifolia) with minor amounts of Douglas ®r (Pseudotsuga menziesii), trembling aspen (Populus tremuloides), cottonwood (P. balsamifera var. trichocarpa), and paper birch (Betula papyrifera). The understory vegetation is a mixture of shrubs, such as thimbleberry (Rubus parvi¯orus), Prince's-pine (Chimaphila umbellata), wild¯owers [e.g. wild sarsaparilla (Aralia nudicaulis), bunchberry (Cornus canadensis), and round-leaf violet (Viola orbiculata)] as well as minor amounts of oak fern (Gymnocarpium dryopteris) and clubmosses (Lycopodium complanatum and L. dendroideum). We sampled soils from ectomycorrhizosphere of 16 sub-alpine ®r trees with diameter at breast height (DBH) from 12 to 27 cm. Samples from several trees were combined to obtain composite samples of nonectomycorrhizosphere, and ectomycorrhizosphere soils. Ectomycorrhizosphere A (ECS-A) samples were dominated by Piloderma spp., and ectomycorrhizosphere B (ECS-B) by Mycelium radicis atrovirens (MRA) and cottony yellow-brown (CYB) types, and where Piloderma spp. had approximately <2% colonization (Table 1). We selected Piloderma spp. because it is commonly observed on subalpine

®r and its yellow color was readily recognizable in the ®eld. The abundance of Piloderma spp., MRA, CYB and other major ECM morphotypes in each sample is given in Table 1. Soil samples were collected from rootlets carefully traced to the main roots of the subalpine ®r. After veri®cation that the roots were linked to subalpine ®r, roots with predominant Piloderma spp. colonization (ECS-A), and roots exhibiting colonization with other ECM (<2% Piloderma spp) (ECS-B) were collected. Non-ectomycorrhizosphere (N-ECM) soil was collected where rootlets and associated rhizomorphs were visually absent. Ectomycorrhizosphere soil was collected from the <3-mm thick layer of soil that adhered to the rootlets by agitating the rootlets on a 2mm sieve until most of the soil from the roots was collected. 2.2. Soil solution extraction and analyses Six composite samples from each of ECS-A, ECSB, and N-ECM samples were saturated with deionized water at ®eld capacity for three weeks at room temperature. Saturated soil was then placed in centrifuge tubes and spun at 15 000 rpm for 20 min at 48C to extract the soil solution. Soil solution was ®ltered at 0.45 mm and stored at 48C for the determi-

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nation of major cations and anions. Major cations were analyzed using inductively coupled plasma-atomic emission spectroscopy at the Central Equipment Laboratory, UNBC. Phosphate in soil solution was determined in a colorimeter using the stannous chloride method, sulfate content was determined colorimetrically by the turbidimetric method using BaCl2, and chloride concentration was measured by argentometric method through titration using AgNO3 (APHA, 1995). 2.3. Geochemical modeling and availability indexes Saturation index (SI) is a measure of the stability of a mineral in a thermodynamic system. It is de®ned as (Allison et al., 1991) SI ˆ log

IAP K

(1)

where IAP is the ionic activity product and K the solubility product constant for the specific mineral. Saturation index <0.0 means that the mineral is undergoing dissolution or weathering, while SI > 0.0 indicates the stability or the formation of the mineral. The saturation indexes for each of the minerals identified in the clay and sand fractions were calculated using MINTEQA2 (Allison et al., 1991) and SOLMINEQPC (Kharaka et al., 1988). MINTEQA2 was used to calculate the saturation indexes for all minerals except chlorite, where SOLMINEQPC model was used (utilizing the composition of the soil solution as input). The modeling exercises were carried out at 258C and 1 atm pressure and the Davies equation was used to calculate various activity coefficients. The modeling exercises were also used to calculate the activities (and speciation) of the major cations in soil solution. The index of soil K‡ availability, was calculated as 00 K (White, 1997) given by K 00 ˆ

Exch: K p ‰KŠ= ‰Ca ‡ MgŠ

(2)

where K00 includes the Gapon constant and cation exchange capacity of the soil, `Exch. K' is the amount of K in the exchange complex (cmolc kgÿ1), and [ ] denotes concentrations of K‡, Ca2‡ and Mg2‡ in the soil solution. Wolt (1994) suggested that an index of Ca2‡ and Mg2‡ availability could be defined by the

activity ratio, CaAR2‡: Ca2‡ AR ˆ

aCa2‡ aCa2‡ aMg2‡

(3)

where a represents activity of the cations in soil solution. 2.4. Statistical analysis We analyzed the data by one-way ANOVA using StatisticaTM, version 5 (StatSoft Inc., 1995). The distribution of data was checked for normality using the Shapiro±Wilks W-test statistic and for homogeneity of variance using the Levene test. Selected data sets had to be transformed numerically to satisfy the requirements of normality of distribution and homogeneity of variances. Post hoc comparison of signi®cantly different means was made using planned least squares difference test statistics. 3. Results 3.1. Soil solution composition The relative mean contents of cations in soil solution followed the order Ca > K > Si > Fe > Mn > Mg > Al > Na for ECS-A samples, Ca > K > Si > Fe > Mg > Mn > Na > Al for ECS-B samples, and Ca > K > Si > Mg > Fe > Na > Mn > Al for N-ECM samples (Fig. 1). Generally, the concentrations of major cations (i.e. K‡, Ca2‡, Mg2‡, and Na‡) were higher in ectomycorrhizal soil compared to non-ectomycorrhizal samples. The contents of K‡, Ca2‡, and Mg2‡ were higher in ECS-A compared to ECS-B and N-ECM soils while the amount of Na‡ is highest in soil solution extracted from ECS-B samples. Trace elements, such as iron and manganese showed an increasing concentration from N-ECM to ECS-B to ECS-A samples. Likewise, the concentrations of silicon and aluminum in soil solution showed the following trend ECS-A > ECS-B > N-ECM soils and Si/Al ratio of at least 5.0. In all types of soil samples, the relative amounts of phosphate, sulfate and chloride in soil solution followed the order chloride > sulfate > phosphate (Fig. 1). The absolute concentrations of these anions generally showed the trend N-ECM > ECS-A > ECS-B samples.

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Fig. 1. Concentrations selected cations and anions in soil solution extracted from ectomycorrhizosphere (ECS-A and ECS-B) and nonectomycorrhizosphere (N-ECM) soils of subalpine fir. (bars represent standard deviation).

3.2. Stability of soil minerals Chlorite Ð (Mg, Fe, Al)6(SiAl)4O10(OH)8, muscovite Ð K(Si3Al)Al2O10(OH)2, and montmorillonite Ð Mx(Si3Al)Al2O10(OH)2 had calculated SI values <0.0 in the ectomycorrhizal and non-ectomycorrhizal soils of subalpine ®r (Fig. 2). Kaolinite Ð Si4Al4O20(OH)4 had SI values >0.0 in the N-ECM and

ECS-B samples and SI <0.0 in the ECS-A samples. Generally, SI values for the minerals in the clay fractions became more negative from N-ECM to ECS-B to ECS-A samples (Fig. 2). The SI values were <0.0 for albite Ð NaAlSi3O8, anorthite Ð CaAl2Si2O8, and K-feldspars Ð KAlSi3O, and quite similar for all the different soil samples. The SI values were >0.0 for goethite in all the soil solutions and

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Fig. 2. Saturation indexes for selected soil minerals for soil solution extracted from ectomycorrhizosphere (ECS-A and ECS-B) and nonectomycorrhizosphere (N-ECM) soils of subalpine fir. (bars represent standard deviation).

showed a decreasing trend from N-ECM to ECS-B to ECS-A samples. 3.3. Ionic strength, equilibrium pH, and availability of K‡ and Ca2‡ At equilibrium, results of geochemical modeling exercises indicated a signi®cantly higher ionic

strength in the soil solution extracted from ECS-A samples compared to ECS-B and N-ECM samples (Fig. 3). Equilibrium pH of the soil solution were generally lower than the pH measured from 1 : 1 soilto-water ratio, and became more acidic from N-ECM to ECS-B to ECS-A samples (Table 1and Fig. 3). The results of the modeling exercises indicated that metallic cations predominate (>99%) the species of

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Fig. 3. Ionic strength, pH, K00 and activities of K‡, Ca2‡ and Mg2‡ in soil solution extracted from ectomycorrhizosphere (ECS-A and ECS-B) and non-ectomycorrhizosphere (N-ECM) soils of subalpine fir. (bars represent standard deviation).

major cations in soil solution. The chemical activities (a) of the free metals K‡, Ca2‡ and Mg2‡ in soil solution assumed to be in equilibrium with the soil minerals were higher in ECS-A compared to ECS-B and N-ECM samples (Fig. 3). The activities of Ca2‡ and Mg2‡ were lowest in ECS-B samples and did not follow the trend shown in the total composition of the soil solution shown in Fig. 1. The activity of K‡ in soil solution followed the trend ECS-A > ECS-B > NECM samples. The calculated soil K‡ availability, K 00 was highest in ECS-A samples and lowest in ECSB samples (Fig. 3). The availability of Ca2‡ given by CaAR2‡ slightly increased from ECS-A (0.74  0.24) to ECS-B (0.78  0.03) to N-ECM (0.80  0.02) samples. Within each type of soil sample, the activities of the major cations followed the order aCa2‡ > aMg2‡ > aK‡.

4. Discussion The dominance of Ca2‡ in soil solution was in agreement with results from soil solution extracted from similar soil horizon (see, e.g. Wolt and Graveel, 1986; Wolt, 1994; Arocena et al., 1992). This is primarily due to the predominance of Ca2‡ in the exchange complex of most soils. In highly weathered forest soils, such as Ultisols, Ca2‡ may not be the dominant cation in soil solution (Zabowski et al., 1996). The range of mean Ca2‡ concentration in solution from all soil samples was very close to the median concentration of 1.27 mmol Ca2‡ lÿ1 for soils with low-intensity fertility management (Wolt, 1994). The weathering of Ca-feldspars (anorthite) as indicated by SI values <0.0 can supply the soils with available Ca2‡ for the trees.

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The presence of Piloderma spp. in ECS-A samples and MRA-CYB in ECS-B samples might have contributed to the high concentrations of Ca2‡ in ectomycorrhizal samples, because ECMs are known to accelerate weathering of soil minerals including Cacontaining minerals (Jongmans et al., 1997). Also, some ECM morphotypes (e.g. Hysterangium spp.) are known to accumulate high levels of Ca2‡ in hyphae and rhizomorphs (Fogel and Hunt, 1983; Cromack et al., 1979) and upon death or inactivity, release the accumulated Ca2‡ into the contents of Ca2‡ in soil solution. Fogel and Hunt (1983) reported Ca concentration in `active' Hysterangium spp. tissues that are >70x higher compared to `dead and inactive' mycorrhizal tissue. In the future, we would like to collect rhizomorphs of Piloderma spp. and MRA-CYB to gather additional information on the extent to which they accumulate Ca2‡ and other elements. The signi®cantly higher aK in the ECS-A samples compared to ECS-B and N-ECM samples was not consistent with the results of Hinsinger and Jaillard (1993) for soil solution extracted from the rhizosphere of Italian rye grass (Lolium multiforum cv. Lemtal). This might be due to differences in the species of fungus present in the rhizosphere of rye grass and/or the physiology of rye grass and subalpine ®r. The high concentration of Al3‡ (>4 mg lÿ1) in the soil solution of ECS-A samples could also inhibit the uptake of K‡ and cause the high level of K‡ observed in soil solution (April and Keller, 1990). The K00 values for ECS-A samples indicated high levels of available soil K, probably due to the contribution of Piloderma spp. colonization to the high CEC of ECS-A soils. The high aK and K00 in ectomycorrhizosphere soils might also be related to the more negative values of SI for muscovite in ectomycorrhizosphere compared to non-ectomycorrhizosphere soils. Primarily, the enhanced release of K‡ from muscovite in the ectomycorrhizosphere is due to mechanical alterations such as realignment, bending and fracturing of minerals due to pressure exerted by growing roots and associated hyphae and rhizomorph on soil minerals (April and Keller, 1990). Robert and Berthelin (1986) showed micrographs of hyphae probing between mica ¯akes to extract K‡. Weathering of K-feldspars as shown by the SI values <0.0 in soil samples might also be the source of K‡ in soil solution.

The weathering of chlorite by direct removal of Mg2‡ (and iron) from the interlayer of chlorite by ECM might be responsible for the higher aMg2‡ in ectomycorrhizal compared to non-ectomycorrhizal samples. Oxalate produced in ECM is an active agent of mineral weathering, because of its high complexing capability (Robert and Berthelin, 1986; Lapeyrie, 1988). For example, ECM system of Hysterangium crassum in Douglas-®r produced high amounts of oxalate to extract the Fe and Al from andesite (Cromack et al., 1979). Iron extracted by ECM from chlorite might form crystalline goethite as indicated by SI values >0.0 for goethite. Generally, the differential weathering of soil minerals between ectomycorrhizosphere and non-ectomycorhizosphere soils is associated, among others, with acidity. Berthelin (1983) attributed the low pH in the ectomycorrhizosphere to the activities of ECM, such as oxidation of inorganics (e.g. sulfur) and the production of organic acids (e.g. oxalic, carbonic, citric, acetic). Low pH could also result from a high rate of NH4‡ uptake by plants (Marschner et al., 1987) as roots exude H‡ into the ectomycorrhizosphere soil to counteract the depleted positive charge arising from the uptake of NH4‡. The presence of ECM has been reported to enhance the adsorption of NH4‡ and K‡ in coniferous trees (Rygiewicz and Bledsoe, 1984; Rygiewicz et al., 1984). In Douglas ®r stands, Cromack et al. (1979) reported that pH 4.9 in soils colonized by Hysterangium crassum was signi®cantly lower than pH 6.1, measured in uncolonized soil. 5. Conclusions Soil-solution composition from ectomycorrhizosphere and non-ectomycorrhizosphere soils of subalpine ®r (Abies lasiocarpa (Hook.) Nutt.) is dominated by Ca2‡, followed by K‡ then Mg2‡. We found that the concentrations as well as the activities of these cations followed the order ECS-A > ECS-B > NECM. A similar trend is true for K00 , a parameter for the availability of soil K‡. These observations could be related to the more negative SI values (or enhanced weathering) for muscovite, chlorite, anorthite and K-feldspars in ectomycorrhizal compared to non-ectomycorrhizal samples. Low pH from the oxidation of inorganics (e.g. sulfur) and the pro-

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duction of organic acids (e.g. oxalic) in the ectomycorrhizal sample is believed to be responsible for the differential breakdown of soil minerals. Other minerals with SI values <0.0 are kaolinite, montmorillonite and albite. Goethite, an iron oxide mineral may be formed from the iron released from the weathering of chlorite as indicated by the SI values >0.0. This study suggests that ectomycorrhizae play a role in the weathering of soil minerals and the composition of soil solution. In the future, it will be useful to establish the speci®city of ectomycorrhizal morphotypes to the soil minerals. This will allow the practical application of the knowledge, such as in fungal inoculation for improved survival of seedlings. Acknowledgements We would like to acknowledge the Natural Sciences and Engineering Research Council for ®nancial support, and J. Craig, R. Crombie, E. Lagerstrom and Dr. D. Dick for laboratory analyses. References Allison, J.D., Brown, D.S., Novo-Gradac, K.J., 1991. MINTEQA2/ PRODEFA2, A geochemical assessment model for environmental systems: Version 3 User's Manual. Env. Res. Lab., US Env. Prot. Agency, Athens , GA. American Public Health Association (APHA), 1995. Standard methods for the examination of water and wastewater: including bottom sediments and sludges. American Public Health Association, Washington, DC. April, R., Keller, D., 1990. Mineralogy of the rhizosphere in forest soils of the eastern United States. Biogeochem. 9, 1±18. Arocena, J.M., Pawluk, S., Dudas, M.J., 1992. Genesis of selected sandy soils in Alberta, Canada, as revealed by microfabric, leachate-, and soil composition. Geoderma 54, 65±90. Arocena, J.M., Glowa, K.R., Massicotte, H.B., Lavkulich, L., 1999. Chemical and mineral composition of two ectomycorrhizosphere soils of subalpine fir (Abies lasiocarpa (Hook.) Nutt.) in Ae horizon of Luvisol. Can. J. Soil Sci 79, 25±35. Berthelin, J., 1983. Microbial weathering processes. In: Krumbein, W.E. (Eds.), Microbial Geochemistry. Blackwell Scientific, Oxford, UK, pp. 223±262. Courchesne, F., Gobran, G.R., 1997. Mineralogical variations of bulk and rhizosphere soils from a Norway spruce stand. Soil Sci. Soc. Am. J 61, 1245±1249. Cromack Jr., K., Sollins, P., Grausten, W.C., Speidel, K., Todd, A.W., Spycher, G., Li, C.Y., Todd, R.L., 1979. Calcium oxalate accumulation and soil weathering in mats of the hypogeous

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