root and time dependent soil structure formation and its influence on gas transport in the subsoil

8
Root and time dependent soil structure formation and its influence on gas transport in the subsoil Daniel Uteau a, *, Sebastian Kouso Pagenkemper a , Stephan Peth b , Rainer Horn a a Institute of Plant Nutrition and Soil Science, Christian-Albrechts-University zu Kiel, Hermann-Rodewald-Str. 2, D-24118 Kiel, Germany b Department of Soil Science, University of Kassel, Nordbahnhofstr. 1a, D-37213 Witzenhausen, Germany 1. Introduction Soil aeration is one of the most important factors influencing fertility and crop production, as it directly affects respiration processes (Glin ´ ski and Ste ˛ pniewski, 1985). Most dryland plant roots and microorganisms need oxygen supply to avoid hypoxia (Ste ˛ pniewski and Ste ˛ pniewska, 2009). Respiration of microorgan- isms plays a fundamental role for the decomposition of organic matter, degradation of contaminants and regulation of N and C cycles amongst others (Allaire et al., 2008; Brzezin ´ ska et al., 1998; Jones et al., 2004) while roots need oxygen for physiological functions and for nutrient uptake processes, which represents 20– 60% of total respiration (Jia et al., 2006; Kuzyakov, 2002; Zhao et al., 2011). Oxygen concentration gradually decreases with depth (Ste ˛ pniewski and Ste ˛ pniewska, 2009) so respiration activity in the subsoil (in this work, we define subsoil as the depth below the plough layer) depends strongly on gas transport. Two main gas transport mechanisms are present in soils: mass flow (advective flux) and molecular diffusion, the latter being of greater impor- tance under the plough pan (Currie, 1965; Glin ´ ski and Ste ˛ pniewski, 1985; Neykova et al., 2011; White and Kirkegaard, 2010). Also a third gas transport mechanism is known as Knudsen diffusivity. It may happen in very dense clayey soils where the molecules activity free path is much greater than the pore radius in which the Soil & Tillage Research 132 (2013) 69–76 A R T I C L E I N F O Article history: Received 17 November 2012 Received in revised form 7 May 2013 Accepted 10 May 2013 Keywords: RIMs Pores Biological tillage Aeration A B S T R A C T The recovery of soil structure following intensive crop production is essential to maintain good fertility and productivity. It is well known that some crops with specific deep rooting characteristics can improve subsoil structure, but few measurements exist on the time to recovery or direct impacts on gas transport on aeration status, thus we hypothesized that root influence on soil structure formation has a significant impact over aeration. This study examined how far three crops and their different root architectures influenced soil structure and aeration by their ability to generate biopores and cracks. Effects of three crops were investigated: (i) shallow roots (Festuca arundinacea, fescue), (ii) taproot-herringbone (Cichorium intybus, chicory) and (iii) taproot-multibranch (Medicago sativa, alfalfa). They were grown in a Haplic Luvisol in a field experiment near Bonn (Germany) during years 2007–2009. Air diffusion, air permeability and air-filled porosity were analyzed as a function of crop type, crop duration (one, two and three years of continuous cultivation) and soil depth. Results of the diffusion measurements were compared with Buckingham’s and Penman’s estimation functions with respect to continuity and tortuosity indices. At a depth of 75 cm, alfalfa showed more macroporosity than chicory and fescue with means of 13.6%, 2.5% and 3.4%, respectively, and at 90 cm means of 17.8%, 2.3% and 4.4%, respectively. Measurements showed decreasing gas diffusion with depth under chicory and fescue cultivation, whereas increasing diffusion with depth under alfalfa. At 90 cm depth alfalfa significantly improved diffusion with respect to chicory and fescue with means of 0.035, 0.014 and 0.009 respectively. Greater soil structure development under alfalfa was interpreted from higher tortuosity index. Under chicory, higher continuity and lower tortuosity of pores dominated the advective transport. Significant effects were observed after three years of cultivation, which suggests the time needed for structural changes. The structural changes observed are promising to extend these results to other soils with swell/shrink potential. ß 2013 Elsevier B.V. All rights reserved. Abbreviations: D s /D o , relative gas diffusion coefficient; u a , air-filled porosity; K ap , air permeability. * Corresponding author. Tel.: +49 4318805547; fax: +49 4318802940. E-mail address: [email protected] (D. Uteau). Contents lists available at SciVerse ScienceDirect Soil & Tillage Research jou r nal h o mep age: w ww.els evier .co m/lo c ate/s till 0167-1987/$ see front matter ß 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.still.2013.05.001

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Soil & Tillage Research 132 (2013) 69–76

Root and time dependent soil structure formation and its influence on gastransport in the subsoil

Daniel Uteau a,*, Sebastian Kouso Pagenkemper a, Stephan Peth b, Rainer Horn a

a Institute of Plant Nutrition and Soil Science, Christian-Albrechts-University zu Kiel, Hermann-Rodewald-Str. 2, D-24118 Kiel, Germanyb Department of Soil Science, University of Kassel, Nordbahnhofstr. 1a, D-37213 Witzenhausen, Germany

A R T I C L E I N F O

Article history:

Received 17 November 2012

Received in revised form 7 May 2013

Accepted 10 May 2013

Keywords:

RIMs

Pores

Biological tillage

Aeration

A B S T R A C T

The recovery of soil structure following intensive crop production is essential to maintain good fertility

and productivity. It is well known that some crops with specific deep rooting characteristics can improve

subsoil structure, but few measurements exist on the time to recovery or direct impacts on gas transport

on aeration status, thus we hypothesized that root influence on soil structure formation has a significant

impact over aeration. This study examined how far three crops and their different root architectures

influenced soil structure and aeration by their ability to generate biopores and cracks. Effects of three

crops were investigated: (i) shallow roots (Festuca arundinacea, fescue), (ii) taproot-herringbone

(Cichorium intybus, chicory) and (iii) taproot-multibranch (Medicago sativa, alfalfa). They were grown in a

Haplic Luvisol in a field experiment near Bonn (Germany) during years 2007–2009. Air diffusion, air

permeability and air-filled porosity were analyzed as a function of crop type, crop duration (one, two and

three years of continuous cultivation) and soil depth. Results of the diffusion measurements were

compared with Buckingham’s and Penman’s estimation functions with respect to continuity and

tortuosity indices.

At a depth of 75 cm, alfalfa showed more macroporosity than chicory and fescue with means of 13.6%,

2.5% and 3.4%, respectively, and at 90 cm means of 17.8%, 2.3% and 4.4%, respectively. Measurements

showed decreasing gas diffusion with depth under chicory and fescue cultivation, whereas increasing

diffusion with depth under alfalfa. At 90 cm depth alfalfa significantly improved diffusion with respect to

chicory and fescue with means of 0.035, 0.014 and 0.009 respectively. Greater soil structure

development under alfalfa was interpreted from higher tortuosity index. Under chicory, higher

continuity and lower tortuosity of pores dominated the advective transport. Significant effects were

observed after three years of cultivation, which suggests the time needed for structural changes. The

structural changes observed are promising to extend these results to other soils with swell/shrink

potential.

� 2013 Elsevier B.V. All rights reserved.

Contents lists available at SciVerse ScienceDirect

Soil & Tillage Research

jou r nal h o mep age: w ww.els evier . co m/lo c ate /s t i l l

1. Introduction

Soil aeration is one of the most important factors influencingfertility and crop production, as it directly affects respirationprocesses (Glinski and Stepniewski, 1985). Most dryland plantroots and microorganisms need oxygen supply to avoid hypoxia(Stepniewski and Stepniewska, 2009). Respiration of microorgan-isms plays a fundamental role for the decomposition of organicmatter, degradation of contaminants and regulation of N and C

Abbreviations: Ds/Do, relative gas diffusion coefficient; ua, air-filled porosity; Kap, air

permeability.

* Corresponding author. Tel.: +49 4318805547; fax: +49 4318802940.

E-mail address: [email protected] (D. Uteau).

0167-1987/$ – see front matter � 2013 Elsevier B.V. All rights reserved.

http://dx.doi.org/10.1016/j.still.2013.05.001

cycles amongst others (Allaire et al., 2008; Brzezinska et al., 1998;Jones et al., 2004) while roots need oxygen for physiologicalfunctions and for nutrient uptake processes, which represents 20–60% of total respiration (Jia et al., 2006; Kuzyakov, 2002; Zhao et al.,2011). Oxygen concentration gradually decreases with depth(Stepniewski and Stepniewska, 2009) so respiration activity in thesubsoil (in this work, we define subsoil as the depth below theplough layer) depends strongly on gas transport. Two main gastransport mechanisms are present in soils: mass flow (advectiveflux) and molecular diffusion, the latter being of greater impor-tance under the plough pan (Currie, 1965; Glinski and Stepniewski,1985; Neykova et al., 2011; White and Kirkegaard, 2010). Also athird gas transport mechanism is known as Knudsen diffusivity. Itmay happen in very dense clayey soils where the moleculesactivity free path is much greater than the pore radius in which the

D. Uteau et al. / Soil & Tillage Research 132 (2013) 69–7670

molecules are which results in a movement that is not related togas concentration differences (Scanlon et al., 2000).

Frequently, mass flow (and its associated parameter Kap for airpermeability) and diffusive molecular exchange (mostly known asthe ratio between the diffusion in soil and the diffusion of oxygenin free air, i.e. Ds/Do) were related to air-filled porosity as it is themost obvious medium for air transport. Some theoreticalphysically based models were developed to calculate permeabilityand diffusion from air-filled porosity. Ehlers et al. (1995) proposeda solution for water and air conductivity by the combination ofHagen–Poiseuille’s equation and a pore size range, which they usedto calculate the continuity and tortuosity of pores. Blackwell et al.(1990) also proposed a model combining flow quantification ofgranular media, tube-like pores and fissures. A semi-theoreticalmodel proposed by Arah and Ball (1994) tried to categorize air-filled porosity into three classes of functionality: arterial, marginaland remote pores. By closer observation of transient diffusionprocesses, they attributed pore tortuosity and discontinuity to themarginal and remote pore classes. Another semi-empiricalapproach is given by Aachib et al. (2004) that dealt with themodeling of the tortuosity/continuity parameter as related to thewater saturation of pores. Nevertheless, because of the difficulty tomeasure continuity and tortuosity, most models are based onempirical approaches. Many observations lead to equations for therelation of Ds/Do to air-filled porosity, e.g. the well known functionsof Buckingham (1904), Penman (1940) and many summarized inTroeh et al. (1982). Ball et al. (1988) used a general fit based onCurrie’s works (1960) of the form:

Ds

Do¼ aub

a ; (1)

with Ds/Do the relative diffusion coefficient at a given matricpotential, ua the air-filled porosity and a and b two empiricallydetermined parameters. Some physical meaning can be given tothese parameters as in the case of a bunch of parallel continuousand straight pores, both parameters should theoretically receivevalues of 1. When tortuous and disconnected, the exponentincreases and the multiplier decreases as result of less influence ofthe air-filled porosity and higher influence of the pore geometry(e.g. Arthur et al., 2013; Ball et al., 1988; Blackwell et al., 1990;Eden et al., 2011; Groenevelt et al., 1984). Common values areattributed to a and b in literature, for example Buckingham’sexponent b, often related to pore tortuosity (Resurreccion et al.,2008) was held to be 2, while Penman’s multiplier a, often relatedto pore continuity (Marshall, 1959), was given the value of 2/3.

Probably the most difficult problem in air transport predictionis the bimodal nature of the soil pore system (Glinski andStepniewski, 1985). Well aggregated soils show a very large andcontinuous inter-aggregate pore network. This leads to goodaeration even in the subsoil. At a pedon scale under arable fieldconditions, a dense platy structure at the plough pan inhibits gasexchange between the free atmosphere and the subsoil as mostpores are horizontally arranged (Dorner and Horn, 2009). At theintra-aggregate scale, anoxic pockets can be found in soils withsubangular blocky, polyhedral or prismatic structures, due to thedistinct pore-size distribution respect to the soil matrix (Currie,1965; Sexstone et al., 1985; Zausig et al., 1993).

Aeration is influenced by texture, bulk density and air-filledporosity among others (Arthur et al., 2012; Schjønning et al., 1999),but these simple measurements do not account for the complexityof soil structure understood as the arrangement of particles,aggregates and pores (Horn, 1994; Horn and Smucker, 2005). It iswell accepted that improved soil structure results in bettertransport conditions, as a more continuous and branched poresystems develop (Dexter, 2004). Already Grable and Siemer (1968)could observe the influence of soil structure, in terms of bulk

density and aggregate size, on O2 diffusion and its consequencesfor root elongation. They found an optimal air-filled porosity of 12–15% reached faster in non-compacted soils with coarser aggre-gates. This and other examples indicate the high dependence ofadvective flow and diffusion on soil structure parameters related toair-filled porosity and pore geometries. Nevertheless, only fewdetails are known about the spatial geometries of soil porenetworks (Nunan et al., 2006). One process that dominates soilstructure is biological activity, which also influences aeration andhence biological habitat. Plant roots create continuous macroporesby root channel generation and by swell-shrink processes (Rasseand Smucker, 1998). Smaller and more rigid aggregates are formedby new tensile and shear cracks, during wetting and drying cycles,which directly affect soil aeration, while root growth itselfimproves gas and water fluxes after root decay or when the rootsstart to shrink and create voids (Carminati et al., 2009). Great scopeexists to select specific crops in an arable rotation that canregenerate soil structure. Deep rooting plants, such as alfalfa(Medicago sativa L.) or red clover (Trifolium pretense L.) for instance,have been shown by Głab (2008) and Kautz et al. (2010) to alleviatecompaction. Fibrous root systems on the other hand bind surfacesoil but also penetrate to depth through biopores or cracks(McKenzie et al., 2009).

We hypothesized that different root architectures generatedistinctive pore networks, directly influencing soil structure andaeration. The main objective of this work was to investigate theinfluence of different root systems on gas transport processes inthe subsoil. Investigations were conducted on a field trial nearBonn (Germany) with three different crops: fescue (Festuca

arundinacea Schreb., shallow roots), chicory (Cichorium intybus

L., taproot-herringbone) and alfalfa (Medicago sativa L., taproot-multibranch). As soil structural changes were expected to be alsotime dependent, we monitored the effects of these crops after one,two and three years of continuous cultivation. The novelty of thiswork is the analysis of time–crop–depth dependent structureformation and its influence on air transport.

2. Methods

2.1. Field description and soil sampling

The field experiment was established at the experimentalstation Klein Altendorf (685902900 N, 5083702100 E) of the Universityof Bonn in 2007. The climate is characterized by temperate humidconditions with maritime influence. Mean annual temperature is9.6 8C with average rainfall of 625 mm, relatively evenly distrib-uted over the year. Winter rainfall usually exceeds evapotranspi-ration, which leads to a regular replenishment of water storage inthe subsoil. Frequent dry spells occur in summer during thegrowing period and cause high root water uptake from the subsoil.The soil at the field experiment is a Haplic Luvisol (WRB, 2006),characterized by an A-horizon (0–30 cm, silty loam), an E-horizon(30–50 cm, silty loam), a Bt-horizon (50–95 cm, silty clay loam)and a CaCO3 rich C-horizon (silty loam).

Nine precrop treatments were investigated in a randomizedcomplete block design with 60 m2 size plots. The design includedthree crops: alfalfa, chicory and fescue, and three crop durations:one, two and three years of continuous cultivation. Seedingdensities were 25 kg ha�1 for alfalfa, 5 kg ha�1 for chicory and30 kg ha�1 for tall fescue (Gaiser et al., 2012). The precrops weresown in spring 2007, 2008 and 2009, respectively. Treatmentsdesignated for two years and one year of the mentioned crops wereseeded after tillage by mouldboard plough in plots previouslysown with spring rye (in 2007) and oats (in 2008). During theprecrop phase, crops were cut four times a year and neither tillagenor fertilization was made. After the precrop phase, shoots were

D. Uteau et al. / Soil & Tillage Research 132 (2013) 69–76 71

harvested a last time and soil was tilled with a mouldboard ploughto a depth of 30 cm. Roots were not pulled out. Intact PVC soil cores(10 cm high and 10 cm diameter) were extracted in spring 2010 ateach treatment. Six replicate samples were taken at 45, 60, 75 and90 cm depth by a manual stainless steel auger with a randomizeddistribution of soil cores over an area of approximately 1–2 m2.

2.2. Air permeability and gas diffusion measurements

Prior to conductivity and gas diffusion measurements, the soilcores were saturated with water from beneath to (assuresaturation of finer pores), then drained and weighed at a matricpotential of �6 kPa, to quantify air-filled porosity (Ball et al., 1988).A steady state method was used to determine air conductivity. Aconstant air flux through the sample was set at a low standardpneumatic pressure difference of 0.1 kPa. A flow measure devicewith a float contained within a tapered hole was used to measurethe flow rate. The float moves up and down as flow passes throughthe flow meter (for more details on the method refer to Peth, 2004).Conductivity was calculated by Darcy’s Law (2):

Ka ¼rigqLs

As p(2)

where Ka is air conductivity (m s�1), ri is air density (kg m�3), g isgravitational acceleration (m s�2), q is the volumetric flow rate(m3 s�1), A (m2) and L (m) are surface and length of the sample andp (Pa) is the pneumatic pressure applied. No correction forcompressibility of gas was required in Eq. (2) as the appliedpressure was very low and flow was assumed to be laminar. Airpermeability was calculated from air conductivity (3):

Kap ¼Kaha

rag(3)

where Kap is air permeability (m2), Ka is air conductivity (m s�1), ha

is air viscosity (Pa s), ra is air density (kg m�3), and g isgravitational acceleration (m s�2).

For gas diffusion, a double chamber method, first suggested byTaylor (1949) and modified by Ball et al. (1981) was used. The samesoil cores as for air conductivity measurements were installedbetween two closed chambers, one filled with synthetic air and theother with nitrogen, respectively. Oxygen sensors (UNISENSE A/S,Aarhus, Denmark) in each chamber monitored the gas exchangeuntil equilibrium was reached. Ball’s (1981) equation, which is arearrangement of Fick’s second law for non-steady-state diffusion,was used to determine diffusion coefficients (4):

Ds ¼�lnðDC=2 � CeqÞ � V � L

A � t � 2(4)

where Ds is the effective gas diffusion in soil (m2 s�1), DC is theoxygen concentration difference between both chambers (g m�3),Ceq is the final oxygen concentration at equilibrium (g m�3), V isthe chamber volume (m3), L is the core length (m), A is the soil coresurface (m2), and t is time from the start of the experiment (s). It isalso recommended to normalize Ds by the free oxygen diffusioncoefficient in air Do (values of 2.01–2.07 � 10�5 m2 s�1 at 20–25 8Cand 101.3 kPa atmosphere pressure; Glinski and Stepniewski,1985) taken at the same pressure and temperature. This results inthe so-called relative diffusion coefficient Ds/Do, which is alwaysless than one because of the solid phase, tortuosity and limitedconnectivity of air filled pores, retarding gas transport comparedwith that in free air. In this study, Knudsen diffusion wasconsidered negligible, as only the finer porosity (e.g. spacebetween clay plates) could host this mechanism. In our samples,enough air-filled porosity was present for Fickian diffusion, whichwas considered the main factor by large (Allaire et al., 2008).

2.3. Estimation of relative diffusion coefficients and pore geometry

indices

Buckingham’s (1904) function (Eq. (4)) assumes an exponentialrelationship between relative diffusion coefficient and air-filledporosity. The exponent was described as pore tortuosity and fixedat a value of ‘‘2’’:

Ds

Do¼ u2

a (5)

where Ds/Do is the relative diffusion coefficient and ua is air-filledporosity (m3 m�3). The widely known function of Penman (1940)proposed a linear estimation with a multiplier of 0.66 (6):

Ds

Do¼ 0:66 � ua (6)

Measured relative diffusion coefficients and air-filled porositieswere compared with these two functions to look for tendencies onpore structure.

As roots are supposed to generate straight channels and altersoil structure by e.g. generate cracks, it is possible to analyze theireffect over pore networks by the interpretation of parameters likecontinuity and tortuosity. For this purpose, continuity andtortuosity indices were calculated. Ball et al. (1988) proposedPenman’s multiplier as pore continuity index (7) named C1 index.For each pair of measured air-filled porosity and relative diffusioncoefficient, C1 can be calculated by:

C1 ¼Ds

Doua(7)

Two additional continuity indices C2 (8) and C3 (9) werecalculated according to Groenevelt et al. (1984), which describe therelationship between air permeability (3) and air-filled porosity:

C2 ¼Kap

ua(8)

C3 ¼Kap

u2a

(9)

where ua is air-filled porosity (m3 m�3). For connected straightpore systems, C1 values around 1 are expected, as diffusion willincrease proportional to air-filled porosity. This value is mostlyreduced because of tortuosity (increased length of pores) butmainly by disconnected pore volume. For similar pore-sizedistributions and pore continuities between treatments, similarvalues of C2 are expected, whereas only similar pore-sizedistributions are shown by similar values of the C3 index(Groenevelt et al., 1984).

An index of tortuosity can be calculated from Eq. (5) formeasured air-filled porosity and relative diffusion coefficient(Buckingham, 1904; Currie, 1960):

t ¼ log Ds=Do

log ua(10)

2.4. Statistical analysis

Effects of plant species (alfalfa, chicory and fescue), depth (45,60, 75 and 90 cm) and time (one, two and three years ofcultivation) on air permeability, tortuosity and continuity indiceswere tested with non parametric statistics, as data can beconsidered non-normal distributed (Ball, 1981; Groenevelt et al.,1984). Kruskal–Wallis test, followed by multiple pairwise Wil-coxon test (U-test) for mean differentiation was used for thispurpose. For assumed normally distributed variables (diffusivity

Fig. 2. Relation between air permeability and relative diffusion coefficient for all

samples at matric potential of �6 kPa. Regression showed R2 = 0.22.

D. Uteau et al. / Soil & Tillage Research 132 (2013) 69–7672

and air-filled porosity), effects were tested by ANOVA followed bya multiple contrast test. Models were tested for accuracy by meansof the root mean squared error (RMSE). All results were classifiedas statistically significant at P < 0.05. All statistical analyses weredone with the R package (R Development Core Team, 2011).

3. Results

3.1. Advective and diffusive gas transport

Air-filled porosity was affected by the alfalfa treatment (Fig. 1).After three years of cultivation, a significantly greater porosity at60, 75 and 90 cm depth was measured compared with chicory andfescue. At 60 cm, alfalfa (3 years) showed differences to chicoryand fescue, with means of 0.119a, 0.046b and 0.042b m3 m�3

respectively (P < 0.01), whereas at 75 cm the means were 0.136a,0.025b and 0.034b m3 m�3 respectively (P < 0.01) and at 90 cmdepth the means were 0.178a, 0.023b and 0.044b m3 m�3

respectively (P < 0.01).Air permeability, Kap was not influenced by any treatment nor

combination of treatments, depth or time (Fig. 1, P = 0.08 for themodel combining all factors, P = 0.08 combining only crop and timeor crop and depth, P = 0.14 combining time and depth). Intrinsicpermeability did not correspond to the observed gradientsobserved in air-filled pore space (e.g. the marked increase of air-filled porosity with depth under 3 years alfalfa), which indicates ahigh influence of structure effects and connected biopores thatcontributed largely to advective transport.

Fig. 1. Air-filled porosity, air permeability and relative diffusion coefficient for 3

crops and 4 depths at matric potential of �6 kPa. Letters indicate significant

differences on crop duration (upper letters) and depth (lower letters).

Oxygen diffusion was significantly affected by the threetreatments. The soil under alfalfa showed a significant improve-ment in relative diffusion down to 90 cm depth with respect tochicory and fescue (means of 0.035a, 0.014b and 0.009b

respectively, P < 0.01), whereas at 75 cm depth it was higherthan fescue alone (means of 0.024a, 0.013ab and 0.011b, P < 0.01).A decreasing diffusion coefficient (not significant) with depth wasobserved for fescue and chicory treatments, and alfalfa after oneyear, while after three years of alfalfa cultivation there was asignificant increase (Fig. 1). Relative diffusion and air-filledporosity showed some relation, especially observable in the alfalfatreatment in Fig. 1, while air permeability did not. Both variablesrepresent distinct transport mechanisms and only showed a weakcorrelation with each other (Fig. 2).

The duration of the treatments also played a significant role,especially under alfalfa, where the diffusion coefficient decreasedat 45 cm of depth while it increased at 75 and 90 cm depth. Adecrease at 90 cm was observed in the fescue treatment and at60 cm under chicory (Fig. 1).

3.2. Models for gas transport prediction

The relation between diffusion coefficient and air-filledporosity showed a general proximity to Buckingham’s model foralfalfa but less so for the fescue treatment. The chicory treatmentwas better described by Penman’s model (Fig. 3). As shown by theRMSE of the measured data against both models (Table 1), relativediffusion coefficients of alfalfa showed a tendency to follow theBuckingham’s model better with time (RMSE of 0.0159 after oneyear of cultivation to 0.0064 after three years of cultivation).Chicory also showed a change in time, where measured values gotcloser to Penman after three years (RMSE from 0.0275 to 0.0181).The fescue treatment showed conductivities and tortuositiesaround 0.24 and 1.4 after three years, slightly similar toBuckingham’s model (RMSE = 0.0103). The main factors control-ling diffusion for chicory were the straightness (mean tortuosity of1.39) and continuity (mean C1 of 0.33) of a small amount of air-filled pores (Table 1). In general, fescue presented the smallest air-filled porosity and diffusivity compared with the other treatments,with maximal values of Ds/Do of 0.025 (Fig. 3).

3.3. Continuity and tortuosity

Tortuosity was observed to be significantly higher under alfalfacultivation (Table 1). A significant increase in tortuosity after three

Fig. 3. Measured diffusion coefficient as a function of air-filled porosity.

Buckingham’s and Penman’s functions are drawn as reference.

Table 1Tortuosity and continuity indices and root mean squared error of the models for predi

Crop Years Tortuosity Continuity

C1

Alfalfa 1 1.57a (0.17) 0.22a (0.11)

2 1.46a (0.28) a 0.28a (0.25) a

3 1.85b (0.14) 0.16b (0.04)

Chicory 1 1.45a (0.22) 0.29a (0.17)

2 1.44a (0.13) b 0.29a (0.10) b

3 1.28b (0.20) 0.42b (0.22)

Fescue 1 1.48 (0.17) 0.24 (0.13)

2 1.46 (0.20) b 0.23 (0.15) c

3 1.44 (0.26) 0.26 (0.24)

Pa *** ***

Values expressed as geometrical means and standard deviation in brackets. Different lette

letters between rows indicate Wilcoxon differences of crops, n.s. = not significantly diffa Kruskal–Wallis test.** P < 0.01.*** P < 0.001.

D. Uteau et al. / Soil & Tillage Research 132 (2013) 69–76 73

years was observed for alfalfa, whereas we found a decrease underchicory. The diffusive pore continuity index (C1) was significantlygreater in the chicory treatment and a time gradient was visible foralfalfa (decreasing with crop duration) and chicory (increasingwith crop duration).

Most values of the advective continuity indices (C2 and C3) wereclassified as high and very high, according to the five levelcategorization for air permeability proposed by Reszkowska et al.(2011) (Fig. 4). The high values were strongly influenced byconnective macropores. The C2 values showed no differencesbetween treatments, but did in C3, which indicates a significantdistinction on pore-size distribution (Table 1).

4. Discussion

It is well known that the distribution of oxygen, especially in thesubsoil, depends on several factors that allow to differentiatebetween air transport and air-filled porosity. Our results confirmedthe stated hypothesis, as the presented crop-specific rootarchitectures showed distinct pore geometries that evolved intime. Because transport, as well as consumption of oxygen, do notdepend only on air-filled porosity but also on soil structure andpore continuity, a more detailed analysis of the pore functionalitychanges as a function of the crop and time are needed. Rootpresence and microbial activity were observed below 1 m depth(Gaiser et al., 2012), which means that oxygen must be transportedacross the soil, primarily influenced by air-filled porosity (Heardet al., 1988; Iversen et al., 2011). If we analyze our data, we candetect an intense effect of the treatments on gas diffusion beneath75 cm depth. This corresponds to the clay-enriched horizon, whichhas a higher shrinkage/swelling potential than the upper clay-deriched horizons (Yassoglou et al., 1994). It is expected that highwater demanding plants (e.g. alfalfa) can influence the generationof macropores (especially cracks) in clay rich soils because of therearrangement of particles by menisci forces, whereas othertaproot crops with less water demand, such as chicory, mainlyproduce large root channels. This was confirmed by the averageprofile soil water content, which after three years of alfalfa was27.2% in comparison with 33.8% and 31.3% for chicory and fescue,respectively (data measured at the sampling time on April 2010).Our data confirms that alfalfa clearly improves diffusive airtransport in the subsoil in comparison with the other two crops.

Advective transport was not influenced by the treatmentsbecause under pressure gradients almost all flow occurs acrossfew connected macropores. This occurs under consideration of

ction of treatment’s effects over diffusion.

Continuity (mm2� 103) RMSE

C2 C3 Buckingham Penman

4.1 (8.1) 58.3 (238.5) 0.0159 0.0295

1.3 (6.9) 15.7 (88.6) a 0.0164 0.0314

2.2 (4.5) 20.1 (43.5) 0.0064 0.0617

4.0 (5.7) 66.9 (92.6) 0.0157 0.0275

4.6 (10.4) 80.5 (163.1) b 0.0165 0.0222

3.1 (10.0) 87.8 (370.9) 0.0143 0.0181

3.8 (9.0) 70.2 (163.1) 0.0155 0.0207

2.3 (8.2) 40.5 (105.7) b 0.0109 0.0217

2.0 (7.4) 46.5 (440.8) 0.0103 0.0239

n.s. **

rs behind the means indicate Wilcoxon differences between crop duration. Different

erent. RMSE = root mean squared error.

Fig. 4. Groenevelt et al.’s (1984) continuity indices C2 and C3 (mm2) and air-filled porosity (left) and squared air-filled porosity (right). Lines represent isovalues of Kap based on

the categories (proposed in Reszkowska et al., 2011), using values of Kap of 8.59 – 18.74 – 39.05 – 85.91 mm2 for categories very low – low – medium – high – very high

respectively.

D. Uteau et al. / Soil & Tillage Research 132 (2013) 69–7674

Hagen–Poiseuille’s law, hence the influence of the pore radii to thefourth on viscous flux. Diffusion on the other hand, is a muchslower process and takes advantage of the total air-filled porosity(Arthur et al., 2012). Fig. 1 shows that all treatments had someconnected macroporosity that was abundant enough to transportair under barometric pressure differences, whether by highporosity or by high continuity (see discussion of C2 and C3 indicesbelow). Nonetheless, in the subsoil, and especially below theplough pan, barometric events that result in advective transportare less likely to occur and diffusion processes take much moreimportance. Thus, we have to consider total air-filled porosity as avariable too.

How far these crack or macropore formations also coincide withmore pronounced pore continuity and related gas exchange fromdeeper soil horizons is often derived from the continuity values.Horn and Kutilek (2009) and Lipiec et al. (2009) stated that thequantification of pore function changes with time or treatment isbetter derived from intensity values like air permeability or gasdiffusion. The application of bulk density or porosity alone,however, is not valuable to derive treatment effects over time. Ourmeasured diffusivities for alfalfa and chicory followed the classicalprediction models of Buckingham and Penman, respectively. Thishas implications for the interpretation of the tortuosity andcontinuity factors, as they depend on this relationship. Poretortuosity is usually described as a component of pore continuity(Currie, 1960; Resurreccion et al., 2008) and can be estimatedempirically by means of Eq. (4) for each pair of Do/Ds and ua.Tortuosity is especially important if the continuous paths of soilpores are tube-like, which is the case for the chicory treatment(Table 1), where some samples even reached C1 values above 0.8(Fig. 1).

The formation of continuous coarse pores by chicory rootgrowth therefore was described well by the Penman equation,showing a linear relation to air filled porosity (i.e. exponent is near1), which means high continuity and low tortuosity of pores (e.g.wormholes and root paths). For the same soil under alfalfatreatment, tortuosity values near to 2 are frequently associatedwith structure related macropores that result from shrinking-swelling processes. Such newly formed pores form a randomized(but root induced) pore network (Marshall, 1959; Ball et al., 1988).If we classify the various root systems we can also differentiatebetween both taproot crops as they induce specific pore systems.The shallow root crop represented by fescue, however, does notshow any clear tendency for pore geometries, which reflects moreinfluence of random spatial arrangement of pores and textureeffects than root induced air-filled porosity. Our values agree withthose of Pagenkemper et al. (2012) who measured, in the samefield experiment, tortuosities in 70 cm large monoliths, by means

of X-ray computer tomography, for one year of fescue cultivationand two years of alfalfa and chicory. They reported tortuosities thatranged from 1.8 to 4.3 without significant differences betweentreatments, which agree with our results as we found nodifferences after one or two years.

The structure effects discussed above are also confirmed by thecontinuity indices C2 and C3 for advective transport. Most valueswere classified as very high which indicates that advective airtransport occurs through air-filled porosity and especially bioporesand cracks. The ranges proposed here correspond well with thoseproposed in other research, for example by Fish and Koppi (1994),who fixed limits at Kap values of 20 – 50 – 100 – 200 mm2. For theselimits, the C2 and C3 indices are also mostly classified as very high.This is explained by an average density of 400 biopores m�2 (onebiopore each 25 cm2, Perkons, U., 2012, unpublished data from thesame studied field) and a used soil core area of 78.5 cm2. Thus, weshould find 3 biopores core�1 where almost all advective transporttakes place. Groenevelt et al. (1984) used the C2 index as anindicator for similar pore-size distributions and pore continuities,whereas the C3 index is related to similar pore-size distributionsonly. This means that differences between C2 and C3 should relateto differences in pore continuity. Fig. 4 clearly indicates thattreatments differentiated more in air-filled porosity than incontinuity of pores. Table 1 shows a significant differentiation ofchicory and fescue treatments with alfalfa in the C3 index, whichresulted from a significantly greater air-filled porosity underalfalfa. Although continuity C2 is higher under chicory, differenceswere not significant. This result suggests similar advectiveconductivity for all treatments, and thus, a combined effect ofpore-size distribution and pore geometries on Kap for alfalfa. At thesame time, pore continuity played the fundamental role intransport for chicory and fescue (if we consider tortuosity andC1 in the analysis too). Therefore, air-filled porosity (as a capacityindicator) and pore continuity (as functional indicator) maybalance values of intrinsic permeability.

After only three years of cultivation, significant effects of thecrops were observed. The chicory and fescue treatments couldmainly affect the upper 45 cm of depth, which was observed by adecrease in relative diffusion coefficient from 45 to 90 cm. This canbe explained by the dense root system between 40 and 50 cmdepth generated by fescue and, thus, an increased biologicalactivity in the upper layers (Kutschera and Lichtenegger, 1982). Onthe other hand, the alfalfa treatment had a stronger influence atdepths below 60 cm. This was especially evident after three years,when alfalfa roots are suggested to be fully developed (Pietola andSmucker, 1995; Rasse et al., 2000). Alfalfa plants develop amultibranch taproot system at depths below 50 cm, which mayincrease the intensity of shrinking/swelling processes (Rasse and

D. Uteau et al. / Soil & Tillage Research 132 (2013) 69–76 75

Smucker, 1998). These results in high abundance of root-induced-macropores (RIMs) that influence not only air capacity, but alsopore continuity. This is also suggested by the tortuosity values,where a significant increase (=structuring) and decrease wasobserved in alfalfa and chicory, respectively. The C1 index alsoshows significant decrease (more dead end pores) and increase(=straighter pores) for alfalfa and chicory, respectively. Thus, thetime dependency for structure formation has been demonstratedwell by these measurements and confirms the effects of rooting,kind of roots and time for rearrangement of particles duringwetting-drying cycles for this soil. This applies to soils withshrinking/swelling potential, i.e. most soils with more than 15%clay (Larney, 2007) and seasonal weather. These processes arefinally essential for continuous nutrient and water uptake behaviorand more sustainable land use. These and other species of similarcharacteristics in root architecture (e.g. for taproot: Trifolium

pretense, or for shallower root: Lolium perenne and many othergrasses) are usually grown as precrops to improve fertility by theso called biological tillage. Main cash crops (like wheat, maize, oat)can show a higher yield potential and a more homogenous nutrientand water depletion down to deeper depth by growing after theseprecrops (Kirkegaard et al., 2008; Rasse and Smucker, 1998).

5. Conclusions

The main hypothesis could be supported by our data, asporosity, tortuosity and pore continuity were affected by thedifferent root systems tested. Taproot systems (alfalfa and chicory)showed specific pore geometries associated with structure relatedair-filled porosity and biopore formation. Alfalfa generated agreater connected air-filled porosity due to more intenseshrinking/swelling processes. Chicory and fescue were not ableto induce significant changes in the subsoil. Our results apply tosoils with shrinking/swelling capacity as the investigated soil(Luvisol) under cultivation of deep rooting crops. Differencesgenerated by alfalfa were observed after three years of cultivation.This suggests that longer time periods are needed for structureformation by root growth and rearrangement of particles, whichhas special meaning if the crops are intended to be used asbiological tillage.

Acknowledgements

Funding of this study by the German Academic Exchange Service(DAAD) and the Chilean National Commission for Scientific andTechnological Research (CONICYT) are gratefully acknowledged.This work was also supported by the German Research Foundation(DFG) within the framework of the research unit DFG-FOR 1320.Authors thank Dr. Hallett for valuable help as well as twoanonymous reviewers and the editor for constructive comments.

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