Rhizosphere effects on soil solution composition and mineral stability

Geoderma 226–227 (2014) 340–347

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Rhizosphere effects on soil solution composition and mineral stability Donald G. McGahan a,b,⁎, Randal J. Southard c, Robert J. Zasoski c a b c

Department of Wildlife, Sustainability, and Ecosystem Science, Tarleton State University, Stephenville, TX 76402, USA Texas A&M AgriLife Research, Stephenville, TX 76401, USA Department of Land, Air and Water Resources, University of California, Davis, Davis, CA 95616, USA

a r t i c l e

i n f o

Article history: Received 30 September 2013 Received in revised form 14 March 2014 Accepted 17 March 2014 Available online 6 April 2014 Keywords: Rhizosphere Clay minerals Mineral stability

a b s t r a c t Rhizosphere properties are known to differ from those of bulk soil, but differences are not always predictable and may be influenced by the kinds of plant roots and by soil mineral composition. Parent material primary minerals have a great influence on the soil secondary mineral suite, and the secondary phyllosilicates can influence soil solution composition. We hypothesized that 1) bulk soil solution and rhizosphere soil solution differ, 2) soil clay mineral Si content, hence parent material mineral composition, controls soil solution Al activity, 3) soil solution composition of soils acidified by agricultural fertilization practices differs from soil solution composition of soils acidified by long-term weathering, and 4) monocots and dicots differ in their rhizosphere effects. We compared the effects of a monocot (fescue, Vulpia myuros) and a dicot (tomato, Solanum lycopersicum) on rhizosphere solution composition in soils with a wide range of Si content. The greenhouse pot experiment was conducted using soils derived from parent materials of sialic, mafic, and mixed lithology. Differences between non-acidified, agriculturally-acidified, and naturally-acidic phases of soil within each parent material were compared so that a soil member of each parent material could be evaluated for its influence on rhizosphere chemistry. Mineral stability diagrams based on soil clay-fraction mineralogy for each parent material type served as guides to interpret rhizosphere effects on soil solution composition. These diagrams demonstrated that rhizosphere solution extracts are farther from equilibrium than are bulk soil solution extracts, that rhizosphere influences are greater in non-acidified than in agriculturally-acidified soils, and that the dicot changed the rhizosphere more than the monocot, relative to bulk soil. The sialic soil diagram suggests that conditions are not favorable for hydroxyl-Al interlayered 2:1 material (HIM) formation in this parent material, presumably because solution Si competes with 2:1 interlayer space for solution Al. The diagrams also suggest a montmorillonite → beidellite → kaolinite transformation in the mafic soil. We can draw no clear conclusions about which solid-phase sink controls solution Al in the non-acidified and agriculturally acidified mixed soils, but SRO aluminosilicate formation may attenuate the Al3+ activity in the naturally acidic soil. © 2014 Elsevier B.V. All rights reserved.

1. Introduction Investigations of rhizosphere soil properties are numerous, and considerable attention has been focused on rhizosphere versus bulk soil pH (Chung and Zasoski, 1994; Chung et al., 1994; Marschner et al., 1986; Nye, 1981; Rollwagen and Zasoski, 1988; Walker, 1960). Rhizosphere pH gradients normal to and along the root axes have been noted by several authors (Blancher and Lipton, 1986; Haussling et al., 1985; Marschner, 1983; Ruiz and Arvieu, 1990). Root and microbial respiration increases acidification in the rhizosphere by formation of carbonic acid (Hinsinger et al., 2003). Because cation uptake often exceeds anion uptake, the rhizosphere often is

⁎ Corresponding author at: Department of Wildlife, Sustainability, and Ecosystem Science, Tarleton State University, Stephenville, TX 76402, USA. Tel.: +1 254 968 9701; fax: +1 254 968 9228. E-mail addresses: [email protected], [email protected] (D.G. McGahan).

http://dx.doi.org/10.1016/j.geoderma.2014.03.011 0016-7061/© 2014 Elsevier B.V. All rights reserved.

also acidified due to proton expulsion for charge balance. On the other hand, the rhizosphere can be less acidic than bulk soil due to NO− 3 uptake in excess of cation uptake. Organic anions are exuded to maintain root charge balance when anion uptake dominates (Marschner et al., 1986; Nye, 1981; Riley and Barber, 1969; Youssef and Chino, 1989). Charge balancing by root exudates as a result of nitrogen anion/cation uptake imbalance is not entirely responsible for rhizosphere pH changes. Independent of nitrogen supply, soil solution nutrient deficiencies, such as Zn, can also affect rhizosphere pH gradients, and Fe deficiencies can result in rhizosphere acidification even in nitrate-fed plants (Marschner, 1995). For plants grown in acidic soils, an increased pH has been demonstrated as a common feature in the apical zone of roots (Marschner, 1995). Solid-phase Al generally dissolves as H+ activity increases (Kerlew and Boulden, 1987; Marschner, 1995) and, solution Al3+ activity is of concern since it may be phytotoxic (Thomas and Hargrove, 1984). Kittrick (1969) proposed the Al2O3–SiO2–H2O system as one that encompasses a large percentage of minerals in soils and noted that mineral

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weathering influences the soil solution, which in turn influences secondary mineral formation. McGahan et al. (2003) suggested that hydroxy-interlayering of 2:1 phyllosilicate minerals plays a large role in sequestration of Al in agriculturally-acidified soil, over a broad range of parent material lithology. The effects of acidification were measurable by selective dissolution and cation exchange studies, but alteration of clay fraction minerals in the acidified soils was not detectable by X-ray diffraction (XRD). Turpault et al. (2005) showed that soil solution from Douglas fir rhizosphere was more acidic and contained more Fe and Al than bulk soil solution, but that Si concentrations in rhizosphere and bulk soil solutions were similar. Calvaruso et al. (2009) showed that the clay-size fractions of rhizospheres of Norway spruce and oak were enriched in Si and depleted in Al and Fe relative to bulk soil as a result of rhizosphere-induced mineral weathering. The rhizosphere is usually a zone of altered pH, Al solubility is strongly pH dependent, and the main source of rhizosphere Al is mineral weathering. Once released from primary mineral weathering, Al complexation by organic acid exudates is likely. Those organic acids, and the Al they complex have three fates: 1) remain in solution, 2) adsorption to the mineral fraction, or 3) consumption by microbes. Interaction of the organic complexed Al, and the complexation itself, is spatially variable with complexation favored proximal to the root tip and lessening longitudinally back from the tip and radially away from the root (Jones, 1998). Rhizosphere organic acid residence time is brief. As degradation of organic acids proceeds, a change in the complicated interplay of competition between organic complexation, Al-hydroxide precipitation, 2:1 mineral interlayers, and reaction with silica to form secondary aluminosilicates is likely. Other cations, pH changes, and variable degradation rate(s) owing to variable organic acid combinations further complicate predictions of Al fates (Jones et al., 2003). Inorganic acids in the rhizosphere are expected to be higher than the bulk soil, but are also difficult to quantify spatially within the rhizosphere itself owing to differential root respiration longitudinally and differential diffusion away from the root. Interpretation of soil–rhizosphere–plant interaction is further complicated by variations in the methods used to sample the rhizosphere. Rhizosphere soil is often collected by agitating plant roots and their associated volume of soil. Soil adhering strongly to the roots after agitation is considered to be rhizosphere soil, and the easily removed soil is designated as bulk soil (Riley and Barber, 1969, 1971). We propose that characteristics of rhizosphere soils are averages in time and space. For example, soil initially at the root apex is associated with zones of elongation, maturation, and finally, mature regions as root growth progresses. Rhizosphere soils sampled as described by Riley and Barber (1969, 1971), are averages that homogenize gradients that were present radially. Differences in soil pH found from root apices through the mature zone, and between primary and lateral roots, are also averaged in this method. Clearly, the rhizosphere is a zone of altered soil properties that is distinct from bulk soil, but collecting samples by agitating extracted roots probably obscures or averages property gradients that may exist. Nonetheless, even having these average differences between bulk and rhizosphere soil should be helpful in investigating the affects of mineral weathering and mineral stability in the rhizosphere. Therefore, we produce “rhizosphere soil” by repeated cropping and mixing of soil material. We compare the solution chemistry and mineralogy of this material with bulk material that has not been cropped. We, admittedly, simplify the complicated rhizosphere environment for this line of inquiry but feel that we can hypothesize that the effects of roots on soil mineralogy can be elucidated from rhizosphere soil solution composition and that because of greater nutrient uptake, dicots (tomato) have a greater rhizosphere effect than do monocots (fescue). If this is true, then do monocots and dicots have different rhizosphere influences? And more generally, are rhizosphere effects on clay mineralogy different in contrasting soil mineral compositions? Specifically, do silicarich parent materials favor aluminosilicate short-range-order formation?

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2. Materials and methods To answer these questions, we produced reasonably large quantities of rhizosphere soil material by repeated cropping of soil materials in a greenhouse experiment, then extracted and analyzed solution from rhizosphere and bulk soil samples (not cropped in the greenhouse) collected from agriculturally-acidified, naturally-acidic, and non-acidified soils. These samples were collected from soils formed in alluvium derived from dominantly sialic, mafic, and mixed lithology. Soil solution composition was compared to mineral equilibrium calculations to assess whether soil solutions were in equilibrium with the solid phase. 2.1. Field Soils were sampled in California, USA to represent non-acidified, naturally-acidified, and agriculturally-acidified soil formed from sialic, mafic, and mixed alluvial parent material (Table 1). Agriculturallyacidified soils were acidified in the field by long-term application of ammonia-based fertilizers (i.e., not experimentally). Agriculturallyacidified soils sampled in tree crop locations were generally sampled in fertigation emitter basins; however, in the case of the mafic soil, samples were collected from the area between trees within the tree row. In tree crops on the mafic and mixed soils, the non-acidified and agriculturally-acidified soils were sampled within 1 to 3 m of each other. Generally, subsurface B horizon samples were used to reduce effects from organic matter and residual surface amendments, but surface horizons were sampled for the agriculturally-acidified and non-acidified mafic soils. 2.2. Soil preparation and properties The fine-earth fractions of the soils were air-dried, lightly crushed via mortar and pestle, and separated from the coarse fraction by passing through a 2-mm sieve. Water contents were determined for the air-dry fraction by oven drying and by the pressure plate method at 33 or 10 kPa, according to texture, to serve as a proxy for field capacity (National Soil Survey Center, 1996). Initial soil reaction (pH) was determined in water (1:1 soil to water). Clay fraction mineralogy was determined by XRD as described in McGahan et al. (2003) and summarized in Table 2. 2.3. Generation of rhizosphere soil Each of the soils in Table 1 was planted to tomato (Solanum lycopersicum), fescue (Vulpia myuros), and no planting (control) in twenty-four, 140-cm3 pots, and grown for eight weeks in the greenhouse until the roots completely exploited the soil volume. No fertilizer was applied, and the plants were watered with deionized water. After each cropping, the soil was allowed to dry, and the roots were separated from the soil. The soil was replanted into the same pot for each replanting. The soil was cropped for three croppings. Pots that never experienced three croppings due to failure of growth were excluded from analyses. This method allowed the plants to repeatedly exploit the same soil volume and generate a rhizosphere-like soil throughout the pot. This technique was employed, rather than the agitation method, in order to generate sufficient quantities of soil for subsequent extraction studies. The assumption was that the entire soil volume was at some time “in intimate contact” with the plant root and, therefore, could be considered as “rhizosphere soil”. After the final cropping, soil material from each pot, including the controls, was air-dried and placed in a perforated nylon holdup cup with Whatman #1 filter paper and brought to 33 or 10 kPa, according to texture, water content (a proxy for field capacity), covered loosely with plastic and allowed to equilibrate for 24 h. After equilibration the holdup was fitted to a nylon receiving cup and centrifuged in a GSA

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Table 1 Classification, location, current crop, and modal pH of soils used in the study. All sites located in California, U.S.A. Soil mapped as classification

County

Parent material

Current vegetation

Condition

pH 1:1 soil:water

Dinuba series coarse-loamy, mixed, superactive, thermic typic haploxeralf Hilmar series sandy over loamy, mixed, superactive, calcareous, thermic aeric halaquept Montpellier series fine-loamy, mixed, superactive, thermic typic haploxeralf Vina series coarse-loamy, mixed, superactive, thermic pachic haploxeroll Vina series coarse-loamy, mixed, superactive, thermic pachic haploxeroll Sites series fine, parasesquic, mesic xeric haplohumult Arbuckle series fine-loamy, mixed, superactive, thermic typic haploxeralf Arbuckle series fine-loamy, mixed, superactive, thermic typic haploxeralf Red bluff series fine, kaolinitic, thermic ultic palexeralf

Stanislaus Stanislaus

Sialic Sialic

Row crops Almonds

Non-acidified Agriculturally-acidified

7.78 5.35

Stanislaus Tehama Tehama Plumas Colusa Colusa Shasta

Sialic Mafic Mafic Mafic Mixed Mixed Mixed

Annual grasses Walnuts Walnuts Mixed conifer Almonds Almonds Pasture

Naturally-acidic Non-acidified Agriculturally-acidified Naturally-acidic Non-acidified Agriculturally-acidified Naturally-acidic

5.23 6.26 5.55 4.55 6.54 3.94 4.67

rotor at 9500 rpm (14,680 G, ~ 31 MPa) for 120 min to force solution from the bottom of the upper unit into the lower collection vial. Pore water pH was measured 12 and 16 h after extraction to allow time for CO2 to equilibrate with the soil solutions. Total dissolved Si and Al concentrations were measured using ICP spectrometry. Statistical analysis was performed using a one-way ANOVA for each dominant soil parent material and acidification type. Tests for the interactions were performed using ANOVA, and a post-hoc Fisher's least-significant-difference test was used for pair-wise comparisons among means. All statistical analyses were performed at a p = 0.05 significance level using SYSTAT for Windows, Version 9 (SYSTAT Inc., Chicago, IL).

The common negative log values of averaged solution concentrations for Ca, Mg, and K extracted from the bulk soils were 2.40, 2.68, and 1.78, respectively. These concentrations were used for montmorillonite, hydroxy-interlayered-material (HIM), and beidellite stabilityequilibrium lines. Two smectites, montmorillonite and beidellite, were chosen because thermodynamic data are available, and because these two phases demonstrate the effect of smectite compositional variation on the interpretation of smectite stability–equilibrium. Montmorillonite is expressed as pH-1/3Al3+ = 0.73 + 0.096pMg2+ + 0.043pFe3+ + 0.74pH4SiO4 − 0.3pH. The calculated beidellite solubility is expressed as pH − 1/3pAl3+ = 1.27 + 0.0024pMg2+ + 0.52pH4SiO4 − 0.047pH.

2.4. Stability diagrams

3. Results and discussion

Mineral stability diagrams were constructed with a gibbsite, kaolinite, quartz, and amorphous silica depicted across all parent materials and phases of acidification thereby allowing easy comparison among the diagrams. The mineral assemblages of the three parent material types differed. Therefore mineral stability lines representative of each particular parent material lithology were added, as needed, to the stability–equilibrium lines for gibbsite, kaolinite, quartz, and amorphous silica to reflect the differences in mineral composition among the parent materials. Mineral stability relationships between the solid and solution phases were based on techniques developed by Kittrick (1969). Thermodynamic values (ΔGof ) used for soil minerals are presented in Table 3. Gibbsite solubility is expressed as pH-1/3pAl = 2.69 and kaolinite solubility as pH-1/3pAl = 1.43 + 1/3pH4SiO4. Iron activity was assumed to be controlled by the relationship pFe3+ = 3pH − 0.49 using Norvell and Lindsay's value for Fe(OH)3 [soil iron] (1981), which is reasonable, because the soils are nominally well drained.

3.1. Stability diagrams and mineral assemblages

Table 2 Mineralogy of the clay fraction from soils used in this study. Parent material

Acidification phase

Dominant mineral

Kaolinite and mica were dominant clay minerals, and vermiculite was a subdominant clay mineral in the soils formed in sialic alluvium (Table 2). Therefore no additional stability–equilibrium lines were added to Fig. 1. In the mafic, non-acidified and agriculturally-acidified bulk soil clay fractions the dominant mineral phase was smectite with a minor contribution of kaolinite. However, in the naturally-acidic, mafic, bulk soil clay fraction, the dominant minerals were halloysite, gibbsite, and goethite (Table 2). Although McGahan et al. (2003) identified smectite as the dominant clay mineral of the mafic parent material, the species of smectite was not identified. Here, we include beidellite and montmorillonite as solid-phase components of the mafic parent material soils depicted in Fig. 2, and these lines serve to underscore the effect of the variability in stability–equilibrium lines of smectite species. Smectite stability– equilibrium varies with pH, and the stability–equilibrium lines were Table 3 Thermodynamic values used to construct stability-equilibrium lines.

Sub-dominant mineral

Sialic Non-acidified Agriculturally-acidified Naturally-acidic

MI, KK MI, KK MI, KK

VR VR VR

Non-acidified Agriculturally-acidified Naturally-acidic

SM SM KH, GI, GE

KK KK –

Non-acidified Agriculturally-acidified Naturally-acidic

VR, HIM VR, HIM KK

MI MI MI

Mafic

Mixed

MI = mica, KK = kaolinite, KH = halloysite, SM = smectite, VR = vermiculite, HIM = hydroxy-interlayered vermiculite, GI = gibbsite, GE = goethite. From McGahan et al., 2003.

Formula 3+

Al Ca2+ K+ Fe3+ Mg2+ H2O Fe(OH)3 (soil) H4SiO4 Al(OH)3 gibbsite SiO2 amorphous SiO2 quartz Al2Si2O5(OH)4 Kaolinite K0.24Ca0.08(Si3.24Al3.77Fe0.24 Mg0.20) O10(OH)5.79 HIV (HIM) Mg0.2(Si3.81Al1.71Fe3+0.22 Mg0.29) O10(OH)2 Montmorillonite Mg0.167Al2.33Si3.67O10(OH)2 Beidellite

Δ G0f (kJ/mol)

Source

−489.4 −553.5 −282.5 −4.6 −454.8 −237.2 −713.4 −1308.0 −1154.9 −848.9 −856.3 −3783.2 −6846.0

(Robie et al., 1978) (Robie et al., 1978) (Robie et al., 1978) (Robie et al., 1978) (Robie et al., 1978) (Robie et al., 1978) (Norvell and Lindsay, 1982) (Robie et al., 1978) (Robie et al., 1978) (Helgeson et al., 1978) (Robie et al., 1978) (Kittrick, 1966) (Karathanasis et al., 1983)

−5254.3

(Weaver et al., 1971)

−5332.5

(Nesbitt, 1977)

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Fig. 1. Stability diagrams for solutions from non-acidified, agriculturally-acidified and naturally-acidic soils formed in sialic alluviums. The symbols are B = Bulk soil (uncropped); rhizosphere tomato (T), and rhizosphere fescue (F). The numeric values are average solution pH. Bars are standard error of mean. Some error bars fall within the size of the symbol. Lower lines in the diagram are more stable.

drawn based on the 1:1 soil:water pH in the bulk soil of each acidification phase. Vermiculite and hydroxy-interlayered-material (HIM) were identified as dominant crystalline minerals in the mixed parent material (Table 2). HIM stability–equilibrium also varies with pH and, therefore, the 1:1 soil:water pH values measured in the bulk soil for each phase of acidification were used to construct the HIM stability–equilibrium lines for that acidification phase. The mixed mineralogy naturally-acidic soil clay fraction had no vermiculite or HIM detectable by X-ray diffraction. The clay fraction was dominated by kaolinite, with a minor component of mica. 3.2. Sialic parent materials In most cases, acidification of the rhizosphere soil led to greater Al3+ solubility, as expected. The extracts from the tomato rhizosphere were more acidic than solutions from the fescue rhizosphere (Table 4). The significantly greater rhizosphere porewater H+ did not necessarily

Fig. 2. Stability diagrams for solutions from non-acidified, agriculturally-acidified and naturally-acidic soils formed in mafic alluviums. The symbols are B = Bulk soil (uncropped); rhizosphere tomato (T), and rhizosphere fescue (F). The numeric values are average solution pH. Bars are standard error of mean. Some error bars fall within the size of the symbol. Lower lines in the diagram are more stable. The bulk (B) soil pH for each phase of acidification was used to construct the pH dependent Beidellite and Montmorillonite stability–equilibrium line and a higher pH lowers the lines placement on the diagram.

result in significantly greater Al3+. Only the agriculturally-acidified tomato rhizosphere had significantly greater Al3+. Our supposition that the dicot tomato would have a greater effect on clay mineralogy is not clear across the acidification phases of the sialic parent material. The rhizosphere pH trend was to move the pH away from the pH of the bulk soil (Table 4). Rhizosphere pH shifts can lead to destabilizing

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Table 4 Solution chemistry used to construct rhizosphere solution stability-equilibrium diagrams.† Soil Sialic Non-acidified Bulk Fescue Tomato Agriculturally-acidified Bulk Fescue Tomato Naturally-acidic Bulk Fescue Tomato Mafic Non-acidified Bulk Fescue Tomato Agriculturally-acidified Bulk Fescue Tomato Naturally-acidic Bulk Fescue Tomato Mixed Non-acidified Bulk Fescue Tomato Agriculturally-acidified Bulk Fescue Tomato Naturally-acidic Bulk Fescue Tomato †

pH

pAl

pSi

pH-1/3pAl

7.09 ± 0.09 (4) b 6.94 ± 0.02 (18) b 6.67 ± 0.04 (17) a

10.46 ± 0.32 (4) b 10.18 ± 0.09 (18) ab 10.02 ± 0.07 (17) a

2.99 ± 0.03 (4) a 2.99 ± 0.02 (18) a 2.94 ± 0.03 (17) a

3.60 ± 0.18 (4) b 3.54 ± 0.09 (18) b 3.33 ± 0.05 (17) a

5.30 ± 0.12 (6) b 5.20 ± 0.04 (24) b 5.06 ± 0.02 (31) a

10.22 ± 0.09 (6) ab 10.39 ± 0.06 (24) b 10.03 ± 0.08 (31) a

2.99 ± 0.05 (6) b 2.95 ± 0.02 (24) b 3.08 ± 0.02 (31) a

1.89 ± 0.13 (6) ab 1.73 ± 0.04 (24) b 1.71 ± 0.04 (31) a

4.97 ± 0.10 (7) a 5.35 ± 0.09 (14) b 4.83 ± 0.06 (16) a

10.92 ± 0.28 (7) b 10.32 ± 0.13 (14) a 10.09 ± 0.08 (16) a

2.93 ± 0.05 (7) ab 3.00 ± 0.03 (14) b 2.89 ± 0.03 (16) a

1.32 ± 0.06 (7) a 1.91 ± 0.10 (14) b 1.46 ± 0.06 (16) a

5.88 (1) 6.22 ± 0.03 (19) b 5.96 ± 0.02 (16) a

10.52 (1) 10.43 ± 0.08 (19) b 10.10 ± 0.05 (16) a

3.61 (1) 2.97 ± 0.01 (19) b 2.84 ± 0.01 (16) a

2.37 (1) 2.73 ± 0.06 (19) b 2.59 ± 0.03 (16) a

5.50 ± 0.06 (6) a 5.68 ± 0.02 (19) b 5.66 ± 0.03 (16) b

10.20 ± 0.19 (6) a 9.79 ± 0.08 (19) b 9.79 ± 0.09 (16) b

2.76 ± 0.01 (6) c 2.83 ± 0.01 (19) b 2.72 ± 0.01 (16) a

2.09 ± 0.09 (6) a 2.41 ± 0.04 (19) b 2.39 ± 0.05 (16) b

5.57 ± 0.03 (6) b 6.12 ± 0.08 (5) a 5.96 ± 0.02 (18) a

10.86 ± 0.10 (6) a 10.48 ± 0.24 (5) a 10.61 ± 0.07 (18) a

4.40 ± 0.01 (6) b 4.00 ± 0.26 (5) a 4.01 ± 0.02 (18) a

1.95 ± 0.03 (6) b 2.62 ± 0.13 (5) a 2.43 ± 0.06 (18) a

5.88 ± 0.04 (5) b 5.85 ± 0.03 (17) b 5.46 ± 0.03 (14) a

10.43 ± 0.12 (5) b 10.83 ± 0.09 (17) a 11.03 ± 0.07 (14) a

3.19 ± 0.03 (5) a 2.93 ± 0.01 (17) b 2.85 ± 0.02 (14) c

2.39 ± 0.05 (5) b 2.23 ± 0.05 (17) b 1.78 ± 0.04 (14) a

4.58 ± 0.00 (3) a 4.73 ± 0.04 (19) a 4.55 ± 0.04 (17) a

10.54 ± 0.09 (3) a 10.50 ± 0.04 (19) a 10.36 ± 0.04 (17) a

3.06 ± 0.02 (3) b 2.88 ± 0.01 (19) a 2.85 ± 0.01 (17) a

1.06 ± 0.02 (3) ab 1.22 ± 0.04 (19) b 1.08 ± 0.05 (17) a

4.18 ± 0.03 (4) ab 4.49 ± 0.47 (2) b 4.08 ± 0.16 (2) a

9.59 ± 0.19 (4) ab 10.23 ± 0.55 (2) b 9.74 ± 0.49 (2) a

3.38 ± 0.01 (4) b 2.95 ± 0.02 (2) a 2.90 ± 0.02 (2) a

0.98 ± 0.04 (4) b 1.07 ± 0.29 (2) b 0.83 ± 0.00 (2) a

Means ± SE (n) in a given, parent material source, acidification status and element followed by the same letter are not significantly different; p = 0.05.

conditions for the dominant bulk soil mineralogy resulting in dissolution of the minerals, and potentially, nutrient release. If the solution were at equilibrium with a crystalline species it would lie on the stability–equilibrium line. Rhizosphere chemistry differences exist between the non-acidified and agriculturally-acidified soil acidification phases. The sialic non-acidified bulk and rhizosphere soil solutions are supersaturated with respect to kaolinite [above the kaolinite stability– equilibrium line] (Fig. 1), but undersaturated [below the stability– equilibrium line] with respect to mica stability–equilibrium. The mica equilibrium is above the diagram boundary and is not shown in Fig. 1. Though mica and kaolinite are co-dominant in the non-acidified sialic soil (Table 2), the rhizosphere solution pH-1/3pAl trend is away from equilibrium with the primary mineral, mica, and toward equilibrium with the secondary mineral kaolinite; as expected. The agriculturally-acidified soil extracts, including the bulk soil, are undersaturated with respect to kaolinite (and mica, Fig. 1). This indicates that both mica and kaolinite are unstable and subject to dissolution. As with the naturally-acidic rhizosphere solution, the agriculturallyacidified rhizosphere pH-1/3pAl trend is also away from the stability– equilibrium line of mica. However, the agriculturally-acidified rhizosphere solution pH-1/3pAl trend is also away from kaolinite (Fig. 1). We hypothesized that effects of roots on soil mineralogy were predicated on altered pH, and that Al solubility is strongly pH dependent. Although the Al concentration did not increase greatly in the tomato rhizosphere and the naturally-acidic fescue, the Si activity did not decrease (Table 4). In a sialic parent material where sources for Si are abundant, one attenuation on solution Al activity might be formation

of amorphous short-range-order (SRO) aluminosilicate species analogous to allophone or imogolite. This cannot be confirmed with the rhizosphere chemistry activity changes in this study. The analytical techniques of McGahan et al. (2003) were also not refined enough to provide direct evidence of the presence of SROs. As the primary mineral mica undergoes alteration, a vermiculite product can play a role in rhizosphere solution Al activity. Aluminumhydroxides precipitating as poly-Al-hydroxide interlayering is a potential sink for Al (Jackson, 1963). An alumino-hydroxy interlayered stabilityequilibrium line, not drawn in Fig. 2, would be slightly lower than kaolinite at the measured pH's. If present, not enough of hydroxyinterlayered-material existed to be detected by x-ray diffraction by McGahan et al. (2003). We cannot confirm that this silica-rich parent material favors aluminosilicate short-range-order formation. We discuss HIM formation further when the mixed parent material results are presented below. Our expectation that the dicot tomato would exert a greater influence on the rhizosphere due to higher nutrient uptake demand does not always hold for the sialic soil. This may be due to our choice of the cultivar of fescue selected (Zorro) as our monocot plant. Zorro Fescue is known to grow well under acidic soil conditions (Kay et al., 1981). We did not assess the vigor, or compare biomass production, between the tomato and fescue. Nonetheless, because the fescue is better adapted than tomato to the lower pH soil conditions in the naturallyacidic soil, it seems reasonable that the fescue exerted a greater influence in the rhizosphere because it tolerated the more acidic conditions better than the tomato.

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3.3. Mafic parent materials The rhizosphere soil solution extracts have lower H+ and greater Al3+ than the bulk soil in all acidification phases. Together this results in a significantly increased pH-1/3pAl in the rhizosphere for all acidification phases (Table 4). The non-acidified bulk solution pore water chemistry is undersaturated with respect to both smectites and the kaolinite. The rhizosphere was supersaturated with respect to both smectites (Fig. 2). The bulk soil, non-acidified, pore water chemistry generally is close to agreement with the X-ray diffraction-determined smectite and kaolinite clay fraction minerals except that the porewater chemistry was under the kaolinite stability–equilibrium line [undersaturated], but smectite was the dominant mineral. Therefore, the montmorillonite stability–equilibrium line probably does not correctly reflect the crystal chemistry of this soils' smectite, which likely intersects with the kaolinite stability–equilibrium line at a higher silica activity. The bulk soil pore water chemistry was undersaturated, but the solution extracts were near the montmorillonite stability–equilibrium line. The solution was also undersaturated [below the stability–equilibrium line] with respect to kaolinite and farther from equilibrium with kaolinite than it was with montmorillonite (Table 4). This is due to the greater stability of montmorillonite at greater Si contents (Fig. 2). The porewater chemistry in the rhizosphere were supersaturated [above the stability-equilibrium line] with respect montmorillonite. With respect to beidellite what was very undersaturated in the bulk soil changed to supersaturated and nearer the stability-equilibrium (Table 4). This is discussed later together with the agriculturallyacidified soil below. Agriculturally-acidified solution silica activity in the tomato rhizosphere sample increased significantly, compared to the bulk soil, but the increase was not as pronounced as in the non-acidified soil. These rhizosphere solutions exhibited increased Al3+, while the H+ decreased (Table 4). This lower H+ activity was observed despite an increase in the solution Al3+ and not in agreement with our expectation that H+ and Al3+ activity changes would be strongly coupled. The agriculturally-acidified bulk solution extracts are supersaturated [above the stability-equilibrium line] with respect to montmorillonite (Fig. 2 and Table 4). Rhizosphere solutions are also supersaturated with respect to montmorillonite and kaolinite, but undersaturated [below the stability-equilibrium line] with respect to beidellite. The formation of SRO aluminosilicates was proposed by McGahan et al. (2003) as a mechanism for controlling solution Al and Si activities in acidified soils. Karathanasis and Hajek (1983) proposed a montmorillonite → beidellite → kaolinite transformation in acid soil systems. The alteration of montmorillonite to beidellite requires an increase in structural Al; a reasonable alteration in acidic soils that is represented by: Mg0.2(Si3.81Al1.71Fe3+0.22 Mg0.29)O10(OH)2 + 0.62Al3+ + 0.56H2O = Mg0.17Al2.33Si3.67O10(OH)2 + 0.32 Mg2+ + 0.22Fe3+ + 0.14H4SiO4 + 0.56H+. The standard free energy change (ΔGf°) for this montmorillonite to beidellite transformation, calculated using the thermodynamic data in Table 3 is positive (28.4 kJ), suggesting the transformation is not spontaneous. The thermodynamic data used to calculate equilibria for smectite in this paper are not specific to the soil and are undoubtedly not correct for the smectite present in our soil. In evaluating smectite stability in naturally acidic soils, Karathanasis and Hajek (1983, 1984) described a soil (Lee) that exhibited different apparent equilibria in the B than in the C horizon. The more stable smectite was associated with the C horizon and the less stable smectite associated with the B horizon. Contributions of Si from mineral dissolutions in overlying horizons can increase smectite stability if Si activity is increased in underlying horizons. In our experiment, leaching the growth pots was generally avoided in the production of rhizosphere soil. Therefore, we did not necessarily simulate field conditions with respect to Si loss. It is reasonable to assume that the non-acidified and agriculturally-acidified solutions

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have somewhat greater H4SiO4 activities than experienced in the field because the soil materials were collected from surface horizons, which would likely experience significant leaching in the field with irrigation. The transformation from beidellite to kaolinite proposed by Karathanasis and Hajek (1983), adapted to the beidellite formula used in this paper, is H+ consuming and results in the release of Si4+ and Al3 + according to the equation: Mg0.167Al2.33Si3.67O10(OH)2 + 2H2O + 7.33H+ = 1/3Al2Si2O5(OH)4 + 1.67Al3 + + 3H4SiO4 + 0.167 Mg2+. At the H+ activities measured in this study, the smectite beidellite is less stable [stability–equilibrium line lies above] than montmorillonite. Furthermore, equations representing smectite equilibria highlight the sensitivity of smectite to pH change (montmorillonite more so than beidellite). Higher pH favors smectite stability (Fig. 2). Barshad (1964) proposed that active cation uptake by plants might favor kaolinite formation, while inactivity would favor montmorillonite. Therefore, differences in cation accumulation by plant roots cause soil solution composition to vary and to favor either montmorillonite or kaolinite stability. Tomato growth altered the solution chemistry more than fescue growth with respect to bulk soil mineralogy only in the agriculturallyacidified soil. This supports our reasoning that because of greater nutrient uptake, dicots (tomato) have a greater rhizosphere effect than do monocots (fescue), but this was not true of the non-acidified or naturally acidic soil (Table 4). 3.4. Mixed parent materials The mixed parent material rhizosphere effects on pore water H+ and Al activity relative to the bulk soil varied. The non-acidified pH decreased in the rhizosphere, but the decrease was only significant in the tomato. Counter to the general notion that Al3+ activity is strongly H+ activity dependent and that they increase, or decrease, together, the tomato and fescue rhizosphere Al3+ activity decreased despite H+ activity increase (Table 4). Neither the agriculturally-acidified, nor the naturally-acidic, rhizosphere pH changed significantly from the bulk solution. However, the naturally-acidic rhizosphere pH were significantly different from each other, and the fescue rhizosphere Al3 + concentration decrease from the bulk soil activity was significant (Table 4). Generally the solutions were undersaturated with respect to kaolinite and HIM (Fig. 3 and Table 4). In the non-acidified soil, the bulk and fescue rhizosphere solutions are above [supersaturated] and on the HIM stability–equilibrium line, and the tomato rhizosphere soil is undersaturated [below the stability–equilibrium line] with respect to the HIM (Fig. 3 and Table 4). An interesting trend in the agriculturally-acidified rhizospheres was one toward increased pH-1/3pAl when compared to the bulk soil. The naturally-acidic fescue increased but the tomato rhizosphere decreased. The fescue rhizosphere pH increased, and the tomato rhizosphere pH decreased in both acidification phases. Except for the agriculturallyacidified tomato, the rhizospheres pAl increased. The pH of bulk soil in these acidification phases was well below 5 (Table 4). This result is counter to the general tendency for the rhizosphere to become acidified, and may be evidence that Al is being sequestered as an alumino-hydroxy interlayer in a 2:1 mineral. As determined by X-ray diffraction the sialic parent material had a subdominant amount of vermiculite, and mica and kaolinite were co-dominant minerals. In this mixed parent material the mica is subdominant and in the acidified soils vermiculite and HIM were co-dominant (Table 2). Therefore, these mixed soils have a greater proportion of vermiculite and HIM than do the sialic soils, thereby providing a sink for solution Al. The changes in rhizosphere pH and pAl in the agriculturally-acidified soil were not statistically significantly different from the bulk soil (Table 4). No clear conclusions can be drawn about what sinks could influence attenuation of Al with acidification in the non-acidified and agriculturally acidified mixed soils. We speculate that the silica content of 3+

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It is clear from Fig. 3 that increasing the pH increases the stability of HIM [lowering the line on the pH-1/3pAl] (Fig. 3). Earlier we suggested that our choice of fescue as our monocot may have been a poor one due to fescue's ability to survive in acidic soils. In the sialic parent material, naturally-acidic phase soil (pH 4.97), and the mixed parent material, agriculturally-acidified (pH 4.53), and naturally-acidic soil phases (pH 4.18), the fescue altered the pH of the rhizosphere to more alkaline conditions (pH 5.35, 4.73, and 4.49 respectfully; Table 4). Localized zones of more alkaline conditions are favorable to Al polymerization (Hsu, 1989) and organic complexation (Jones, 1998; Jones et al., 2003). More favorable conditions for organic complexation, Alpolymerization, HIM and vermiculite dominating the clay mineralogy of the agriculturally acidified phase of the mixed parent material soil, suggest that SRO aluminosilicate formation is not a major sink for solution Al. In contrast, in the naturally-acidic phase of the mixed parent material soil, neither vermiculite nor hydroxy-interlayered-material was detected by x-ray diffraction (McGahan, 2003, Table 2). The fescue rhizosphere pH increased, as did the pAl, but in the tomato rhizosphere the pAl increased, while the pH decreased (Table 4). One explanation for the difference between the fescue and tomato rhizosphere is that soluble organic complexed Al is measured as part of the Al pool. In the absence of vermiculite or HIM, it is easier to argue that Al3 + activity could be attenuated by SRO aluminosilicate formation, especially because the silica activity is higher in the rhizospheres than the bulk soil (Table 4). 4. Summary

Fig. 3. Stability diagrams for solutions from non-acidified, agriculturally-acidified and naturally-acidic soils formed in mixed alluviums. The symbols are B = Bulk soil (uncropped); rhizosphere tomato (T), and rhizosphere fescue (F). The numeric values are average solution pH. Bars are standard error of mean. Some error bars fall within the size of the symbol. Lower lines in the diagram are more stable. The bulk (B) soil pH for each phase of acidification was used to construct the pH dependent HIM, stability–equilibrium line and a higher pH lowers the lines placement on the diagram.

the mixed parent material could support SRO aluminosilicate formation, and that alumino-hydroxy interlayering of 2:1 minerals could be an important sink for Al in these mixed parent material soils. Al-organic interactions are also possible, but were not directly assessed in this study. Organic acid complexation of Al competes with Al-hydroxide precipitation, 2:1 mineral interlayers, and reaction with silica to form secondary aluminosilicates. Further complicating the role organo-Al complexation and the competition organic acids bring to aluminum's participation in SRO formation is, that while organics are subject to degradation by microbes, this study had no mechanism to capture variability in type of organic acids produced across the soil plant combinations. Nor did the study have a mechanism to fingerprint changes in the microbial community as a result/response to the plant soil interaction. Furthermore, in the absence of thermodynamic information about the specific minerals in these soils the HIM line is only one possibility.

Our objectives were to determine the effects of roots on soils with contrasting mineralogy and to assess these effects by comparing rhizosphere and bulk soil solution composition with an eye toward Al and Si. We hypothesized that dicots (tomato) would have a greater rhizosphere effect than do monocots (fescue) due to greater nutrient uptake by dicots. Our experimental approach produced rhizosphere soil solutions that were altered with respect to the bulk soil. These solutions are generally under- or super-saturated, and not in apparent equilibrium with the dominant clay minerals in the soils. Rhizosphere soil solutions were commonly enriched in Si with respect to the bulk solutions, though not always significantly so, and solution extracted from tomato rhizosphere samples generally had higher Si concentration than solutions extracted from fescue rhizospheres. Rhizosphere soil solution composition generally reflected the dominant clay mineralogy of the bulk soil, but generally shifted away from the dominant clay mineral stability-equilibrium line. Generally, rhizosphere tomato solutions were further from equilibrium with bulk soil mineralogy than were fescue, partially supporting our thought that the dicot tomato would have a greater influence on the rhizosphere soil chemistry due to more intensive nutrient uptake. Our results show that rhizosphere (as defined here through repeated cropping) effects on soil solution composition are varied and depend on soil mineralogy and the type of plants grown. Generally, the rhizosphere modifies the soil in the rooting environment, making acidic soils less acidic, and making alkaline soils more acidic. These changes affect mineral stability relative to bulk soil, and are not simplistic. Relationships between silica content of parent material and formation of short-range-order aluminosilicates are not easily deduced from pore water chemistry, and mineral thermodynamics are further encumbered by incomplete or unknown thermodynamics for the clay mineralogy in the soils. Kinetics of solution/solid phase interaction must play a big role in controlling reactions, rather than equilibrium relationships. Plotting the pore water chemistry on stability–equilibrium diagrams helped in understanding rhizosphere influences on the soils, but influences of the rhizosphere on specific fates of Al are only suggestive and rather speculative. The sialic soil porewater chemistry suggests that conditions were not favorable for HIM formation in this parent material,

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probably because solution Si competes with 2:1 mineral for interlayer Al or because of complicated organo-Al relationships. The porewater chemistry suggests a montmorillonite → beidellite → kaolinite transformation in the mafic soil. No clear conclusions can be drawn about which solid phase sink(s) could influence solution Al with acidification in the non-acidified and agriculturally acidified mixed soils, but SRO aluminosilicate formation may attenuate the Al3+ activity in the naturally acidic mixed soil. References Barshad, I., 1964. Chemistry of soil development. In: Bear, F.E. (Ed.), Chemistry of Soil. Reinhold Publishing Corporation, New York, pp. 1–70. Blancher, R.W., Lipton, D.S., 1986. The pe and pH in alfalfa seedlings rhizosphere. Agron. J. 78, 216–218. Calvaruso, C., Turpault, M.P., Leclerc, E., 2009. Rapid clay weathering in the rhizosphere of Norway spruce and oak in an acid forest ecosystem. Soil Sci. Soc. Am. J. 73, 331–338. Chung, J.B., Zasoski, R.J., 1994. Ammonium–potassium and ammonium–calcium exchange equilibria in bulk and rhizosphere soil. Soil Sci. Soc. Am. J. 58, 1368–1375. Chung, J.B., Zasoski, R.J., Burau, R.G., 1994. Aluminum–potassium and aluminum–calcium exchange equilibria in bulk and rhizosphere soil. Soil Sci. Soc. Am. J. 58, 1376–1382. Haussling, M., Leisen, E., Marschner, H., Romheld, V., 1985. An improved method for nondestructive measurements of the pH at the root-soil interface (rhizosphere). J. Plant Physiol. 117, 371–375. Helgeson, H.C., Delany, J.M., Nesbitt, W.H., Bird, D.K., 1978. Summary and critique of the thermodynamic properties of rock-forming minerals. Am. J. Sci. 278-A, 1–229. Hinsinger, P., Plassard, C., Tang, C., Jaillard, B., 2003. Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: a review. Plant Soil 248, 43–59. Hsu, P.A., 1989. Aluminum hydroxides and oxyhydroxides, In: Dixon, J.B., Weed, S.B. (Eds.), Minerals in Soil Environments, 2nd ed. Soil Sci. Soc. Am. (Madison, WI). Jackson, M.L., 1963. Interlayering of expansible layer silicates in soils by chemical weathering. Trans 11th Natl Conf Clays Clay Miner. Pergamon Press, New York, pp. 29–46. Jones, D.L., 1998. Organic acids in the rhizosphere — a critical review. Plant Soil 205, 25–44. Jones, D.L., Dennis, P.G., Owen, A.G., van Hees, P.A.W., 2003. Organic acid behavior in soils — misconceptions and knowledge gaps. Plant Soil 248, 31–41. Karathanasis, A.D., Hajek, B.F., 1983. Transformation of smectite to kaolinite in naturally acid soil systems: structural and thermodynamic considerations. Soil Sci. Soc. Am. J. 47, 158–163. Karathanasis, A.D., Hajek, B.F., 1984. Evaluation of aluminum–smectite stability equilibria in naturally acid soils. Soil Sci. Soc. Am. J. 48, 413–417. Karathanasis, A.D., Adams, F., Hajek, B.F., 1983. Stability relationships in kaolinite, gibbsite, and Al-hydroxyinterlayered vermiculite soil systems. Soil Sci. Soc. Am. J. 47, 1247–1251.

347

Kay, B.L., Graves, W.L., Adams, T.E., Garver, M., Croeni, K., Slayback, R.D., Jan.–Feb. 1981. Zorro annual fescue for emergency revegetation. Calif. Agric. 35, 15–17. Kerlew, P.W., Boulden, D.R., 1987. Chemical properties of the rhizosphere in an acid subsoil. Soil Sci. Soc. Am. J. 51, 128–132. Kittrick, J.A., 1966. The free energy of formation of gibbsite and Al(OH)3 from solubility measurements. Soil Sci. Soc. Am. J. 30, 595–598. Kittrick, J.A., 1969. Soil minerals in the Al2O30SiO2–H2O system and a theory of their formation. Clay Clay Miner. 17, 157–167. Marschner, H., 1983. In vivo measurement of root-induced pH changes at the soil-root interface. Pflanzenphysiol. Bodenkd. 111, 241–251. Marschner, H., 1995. Mineral Nutrition of Plants. Academic Press, New York (889 pp.). Marschner, H., Romheld, V., Horst, W.J., Martin, P., 1986. Root-induced changes in the rhizosphere: importance for the mineral nutrition of plants. Z. Pflanzenernaehr. Bodenkd. 149, 441–456. McGahan, D.G., Southard, R.J., Zasoski, R.J., 2003. Mineralogical comparison of agriculturally acidified and naturally-acidic soils. Geoderma 114, 355–368. National Soil Survey Center, 1996. Soil survey laboratory methods manual. Soil Survey Investigations 42USDA-SCS, Lincoln, NE (Version 3). Nesbitt, H.W., 1977. Estimation of the thermodynamic properties of Na–Ca–Mg– beidellites. Can. Mineral. 15, 22–30. Norvell, W.A., Lindsay, W.L., 1982. Estimation of the concentration of Fe3 + and the Fe3 + (OH)3 ion product from equilibria of EDTA in soil. Soil Sci. Soc. Am. J. 46, 710–715. Nye, P.H., 1981. Changes of pH across the rhizosphere induced by roots. Plant Soil 61, 7–26. Riley, D., Barber, S.A., 1969. Bicarbonate accumulation and pH changes at the soybean (glycene max (L.) Merr.) root-soil interface. Soil Sci. Soc. Am. J. 33, 905–908. Riley, D., Barber, S.A., 1971. Effect of ammonium and nitrate fertilization on phosphorus uptake as related to root-induced pH changes at the root-soil interface. Soil Sci. Soc. Am. J. 35, 301–306. Robie, R.A., Hemingway, B.S., Fisher, J.R., 1978. Thermodynamic properties of minerals and related substances at 298.15 K and 1 bar (10* pascals) pressure and at higher temperatures. Geol. Surv. Bull. 1452 (Washington). Rollwagen, B.A., Zasoski, R.J., 1988. Nitrogen source effects on rhizosphere pH and nutrient accumulation by Pacific Northwest conifers. Plant Soil 105, 79–86. Ruiz, L., Arvieu, J.C., 1990. Measurement of pH gradients in the rhizosphere. Symbiosis 9, 71–75. Thomas, G.W., Hargrove, W.L., 1984. The chemistry of soil acidity, In: Adams, F. (Ed.), Soil Acidity and Liming, 2nd ed. Soil Sci. Soc. Am. (Madison, WI). Turpault, M.P., Uterano, C., Boudot, J.P., Ranger, J., 2005. Influence of mature Douglas fir roots on the solid soil phase of the rhizosphere and its solution chemistry. Plant Soil 275, 327–336. Walker, T.W., 1960. Uptake of ions by plants growing in soil. Soil Sci. 89, 328–332. Weaver, R.M., Jackson, M.L., Syers, J.K., 1971. Magnesium and silicon activities in matrix solutions of montmorillonite-containing soils in relation to clay mineral stability. Soil Sci. Soc. Am. J. 35, 823–830. Youssef, R.A., Chino, M., 1989. Root-induced changes in the rhizosphere of plants. Soil Sci. Plant Nutr. 35, 461–468.