Effects of soil compaction on the relationships between nematodes, grass production and soil physical properties

Applied Soil Ecology 14 (2000) 213–222

Effects of soil compaction on the relationships between nematodes, grass production and soil physical properties L.A. Bouwman a,∗ , W.B.M. Arts b b

a Alterra, Green World Research, P.O. Box 47, 6700 AA Wageningen, The Netherlands DLO Research Institute for Agricultural and Environmental Engineering, P.O. Box 43, 6700 AA Wageningen, The Netherlands

Received 18 October 1997; received in revised form 24 February 2000; accepted 1 March 2000

Abstract As farm machinery has become heavier, concern has grown about its direct effects on soil physical conditions and its indirect effects on crop yields and soil biota. To study the relationships between these parameters, non-grazed temporary grassland plots on a loamy sand soil were subjected to full-width load traffic with widely different loads (0, 4.5, 8.5 and 14.5 t) one to four times per year for a period of 5 years. Soil bulk density was monitored as an indicator of soil compaction. Grass yield was measured throughout the experimental period. Root distribution over the soil profile and nematodes populations were assessed during the final year of the experiment. Results indicate that a moderate degree of compaction (∼4.5 t load) gave the highest crop yield and that at higher degrees of compaction roots failed to penetrate into the deeper soil layers (>20 cm depth). Total numbers of nematodes were not affected by compaction, but their distribution over the various feeding types shifted towards a population with increased numbers of herbivores and decreased numbers of bacterivores and omnivores/predators. This change in the structure of the nematode assemblage is associated with poorer conditions for crop growth. © 2000 Elsevier Science B.V. All rights reserved. Keywords: Grass production; Habitable pore space; Nematode trophic structure; Root distribution; Soil bulk density; Soil compaction

1. Introduction Soil compaction is an important form of physical soil degradation (Van Ouwerkerk and Soane, 1994). The use of heavy load traffic (machinery) in modern agriculture causes substantial soil compaction, counteracted by soil tillage that loosens the soil. Higher soil bulk densities affect resistance to root penetration, soil pore volume and permeability to air, and thus, finally the pore space habitable for soil organisms. Through a combination of these factors, soil compaction will ∗ Corresponding author. Tel.: +31-317-474352; fax: +31-317-424812. E-mail address: [email protected] (L.A. Bouwman)

affect crop growth (Brussaard and Van Faassen, 1994; Soane and Van Ouwerkerk, 1994). Soil pores also accommodate biological processes such as organic matter decomposition and nutrient mineralization (Elliott et al., 1980; Hassink et al., 1993). Also, herbivorous organisms feeding on living plant roots live in the interstitial spaces present in the soil. Conventionally, fields are regularly tilled for arable crop production and the use of heavy load machinery creates a plow layer with increased bulk density, usually below 25 cm depth, and with a decreased bulk density in the upper soil layers. The passage of heavy load traffic on perennial grassland also causes compaction of the upper soil layers but there are no tillage operations to counteract this compaction. In perennial and temporary (ley)

0929-1393/00/$ – see front matter © 2000 Elsevier Science B.V. All rights reserved. PII: S 0 9 2 9 - 1 3 9 3 ( 0 0 ) 0 0 0 5 5 - X

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grasslands, compaction affects many physical and biological soil properties and processes by various direct and indirect mechanisms. To unravel these, we should know the relationships between the load of the passing traffic and the resulting soil compaction, bulk density, root distribution over the soil profile, crop yield, and finally the structure of the community of soil organisms and its functioning. This knowledge may help farmers in their choice of machinery load, the width and the pressure of the tires and the frequency of traffic, depending on soil type, weather conditions, and acceptable degree of compaction (Arts et al., 1994). Nematodes are involved in a wide range of activities and connections to other organisms in the soil food web, comprising species feeding on living roots (herbivores (H)), on microorganisms (bacterivores (B); fungivores (F)), and species feeding on larger organisms (predators (P)) or on mixed diets (omnivores (O)). Nematode communities in permanent grasslands are relatively stable with respect to numbers and have a high species diversity. Numbers of specimens in trophic groups often decrease in the order B>F> H>O/P (Boström and Sohlenius, 1986). The various nematode trophic groups reflect important microbiological and phytopathogenic processes such as organic matter decomposition, nutrient mineralization and herbivory. Although numbers of nematodes belonging to a particular feeding category are not always correlated to the amount of specific food, numbers are correlated with process rates, e.g. numbers of bacterivorous nematodes correlate with bacterial production (Clarholm et al., 1981) and N mineralization rate, in particular, in sandy soils with pore diameters between 30 and 90 ␮m (Hassink et al., 1993), and herbivores correlate with root growth, etc. Soil compaction affects nematodes directly as well as indirectly. Vulnerable species can be damaged during passage of the traffic (Boag, 1985); decreased habitable pore space after passage of the traffic affects probably all taxa except those that are intimately connected with root development, and finally root dynamics in particular affects the numbers of herbivores and some root-generated microbivorous taxa (Griffiths et al., 1991; Bouwman et al., 1993). The effect of tillage and compaction regimes on total numbers and dynamics of nematodes can therefore not be generalized, but feeding categories and taxa should be examined individually (Fortnum and Karlen, 1985; Parmelee and Aston, 1986; Thomas, 1978).

Trophic differences among nematode populations were observed to be indicative of variations in crop yields (Edwards, 1988; Edwards and Kimpinski, 1997) and also of decomposition and, in particular, N mineralization processes (Hassink et al., 1993). A field experiment was carried out to study the relationships between traffic load and physical, biological and (crop) production characteristics of the soil. In 1988 the experiment (Arts et al., 1994) was established on a marine loamy sand soil in The Netherlands, where grass was sown on plots (strips) previously tilled to a depth of 50 cm and consequently subjected to different degrees of soil compaction over the whole surface of the plots. Soil physical characteristics as well as crop yields were measured throughout the 5-year trial period and finally, in the last year of the experiment (1992), the distribution of the roots over the soil profile and the nematode fauna were recorded in two plots with different degrees of compaction. It was hypothesized that compaction may have positive as well as negative effects on crop yield and thus, a site-specific optimum degree of soil compaction exists. Single season changes in soil management regimes have little lasting effect on nematode communities (Baird and Bernard, 1984; Sohlenius and Sandor, 1989), but the nematode fauna in the upper 10 cm of the grass-sod of the experimental plots is assumed to be in a new equilibrium after 4 years of growth under experimental conditions.

2. Materials and methods 2.1. The experimental site The research was carried out at the Oostwaardhoeve experimental farm (longitude 52◦ 180 N, latitude 4◦ 850 E) in the Wieringermeer, a reclaimed polder, used for agricultural production since 1934. The soil is a calcareous loamy (30% silt) marine sand (M50: 50–105), containing 5% organic matter (Arts et al., 1994). 2.2. The establishment of the field experiment In April 1988 an area of ca. 2 ha, 180 m×120 m, was tilled with a rotodigger to a depth of 50 cm to loosen the soil, resulting in a loose layer of 60 cm depth. The field was divided into three blocks of

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equal size, on which four plots (strips) were assigned (180 m×2 m) to four loading treatments: 0, 4.5, 8.5 and 14.5 t. For this purpose, a loading frame with a steel roller, 2 m wide and 1.2 m in diameter, carrying the various loads passed over the plots; the roller was drawn by a tractor with 3 m trail-width. After the first compaction treatment perennial ryegrass, Lolium perenne (mixture BG3) was sown, and harvested up to four times annually. After each harvest the specific traffic loads passed over the various plots. A load of 1 t exerts a pressure of 100–500 kg per dm2 , depending on the actual compactability of the upper soil layer (e.g. dry versus wet conditions). The experiment was extended with different rates of nitrogen fertilization (0, 140, 280 and 420 kg N ha−1 per year) within various subplots. 2.3. Physical measurements Over the period 1988–1992, soil porosity, permeability and penetrability were reduced. To characterize the soil condition, measurements were carried out at different depths, after each harvest: thickness of the initially loosened layer, soil bulk density, penetration resistance, and the soil moisture content (measured weekly). To measure the thickness of the loosened layer, in each plot five tiles (30 cm×30 cm) were buried on top of the undisturbed subsoil, i.e. at a depth of 60 cm, after rotodigging in 1988. The thickness of the soil layer above these tiles was measured as well as the position of the tile with regard to a fixed reference point. This latter measurement was necessary to correct the first one for sinking of the tile. Soil bulk density was measured in the 15–20 and 30–35 cm layers below the soil surface, in undisturbed ring samples containing 100 ml soil. The penetration resistance was measured with a Bush Penetrometer conus type B, ASAE Standards, 1993. This parameter, expressed as average values of 10 penetrations per event in the soil layers 0–5, 5–10, 10–15 cm, etc. indicates the pressures roots have to exert to overcome soil compaction, effective root-zone depth (Gregory, 1988), as well as soil porosity and compaction (Groenevelt et al., 1984). Soil moisture contents (w/w) in different soil layers, including the 0–5 cm layer, were measured weekly in

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mixed samples, originating from 10 subsamples, by overnight drying 20 g soil at 105◦ C. 2.4. Crop measurements Grass yield and distribution of grass roots over the soil profile were measured. Crop responses are likely to be directly related to properties such as pore size distribution, permeability, aeration, etc. and indirectly to bulk density and compaction. Grass dry matter yield was determined after each harvest of 20 m×1.2 m strips. Annual grass yields are the sums of three or four harvests. The distribution of the roots over the soil profile was measured once by the pin-board method (Böhm, 1979) in June 1992, in the 4.5 and 14.5 t treatments, fertilized with 280 kg N ha−1 per year. 2.5. Nematode densities Nematodes were isolated from the soil in 1992, the fifth year of the experiment, in March, June, September, and December, in the 4.5 and 14.5 t treatments (280 kg N). The organisms were isolated from 3×100 g fresh soil from the upper 10 cm with Oostenbrinks’s elutriation method (Jacob and Van Bezooyen, 1984). Total numbers were counted and expressed per 100 g dry soil; the figures presented are averages of three samples. Sixty specimens per sample were identified to genus level and assigned to the following feeding types: bacterivores (Rhabditidae; Cephalobidae, including genera such as Cephalobus, Acrobeloides, Acrobeles, Chiloplacus but also a small number of non-cephalobid Teratocephalidae; Monhysteridae including a small number of Prismatolaimidae; Plectidae; Panagrolaimidae; Alaimidae), fungivores (Aphelenchoididae including mainly Aphelenchoides and few Aphelenchus avenae; Tylenchidae; Psilenchidae), herbivores (Paratylenchidae; Pratylenchidae) and omnivores/predators (Dorylaimidae). 2.6. Statistical analysis Effects of compaction were tested by analysis of variance (ANOVA): all pairwise multiple comparison procedures were carried out according to the Student–Newman–Keuls method.

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3. Results 3.1. Physical measurements The thickness of the initially loosened layer of 60 cm depth had already stabilized during the first year (1988) of the experiment, and only fluctuated seasonally, due to moisture content in the subsequent years. Thickness decreased monotonously with load (from 0 → 14.5 t, it changed from 55 → 43 cm) (Fig. 1a). Soil bulk density, not measured in the sod but in the 15–20 and 30–35 cm depth layers, increased with load treatment during the first 2 years, and subsequently stabilized; in the 0 t treatment (15–20 cm layer) bulk density only increased slightly in the last 2 years of the experiment (1.10 → 1.15 g cm−3 ). In the 4.5 t treatment the bulk density in the 15–20 cm layer increased from 1.10 g cm−3 in the loosened soil in 1988 to 1.41 g cm−3 in 1992. The resistance to penetration in the various soil layers varied between seasons along with soil moisture, with the highest values in summer (dry) and the lowest in winter (wet conditions). The resistance increased in all load treatments from 1988 to 1989 and then stabilized (Fig. 1b).The resistance also increased with soil depth but only in the upper soil layers. Resistance was highest in the 14.5 t treatment and lowest in the 0 t treatment. In the 0–5 cm layer the lowest values were measured in the 0 t treatment in winter 1991, (0.55 MPa) and the highest in the 14.5 t treatment in summer 1991 (4 MPa; Fig. 1b); the latter resistance was much too high to be broken by monocotyledons (Dexter, 1986). Soil moisture content in the 0–5 cm layer showed a considerable increase parallel to the weight of the load-traffic (Fig. 1c). Moisture contents in the 14.5 t treatment were up to 30% higher than in the 0 t treatment. In winter moisture contents in the 14.5 t treatment in the upper 5 cm soil layer approached to 50% (w/w), decreasing down to 10% in summer. 3.2. Crop measurements Above ground dry matter yields as affected by N-application and load-treatment are presented in Fig. 2. The effect of the load-treatment was significant (p<0.01) and the N-response/load-treatment interaction effect was also significant (p<0.01), but

not when values for 368 kg N and 0 t load were left out of the calculations; this means that in practice the loss of yield due to soil compaction was independent of the level of N application (Keen, 1993). In all years, grass yield was highest in the 4.5 t treatment (Fig. 2), on average it was 12,000 kg dry matter per hectare (280 kg N plots) and it was 5, 6 and 12% less in the 8.5, 0 and 14.5 t treatments, respectively (Table 1). The distribution of roots over the soil profile differed significantly between the 4.5 and 14.5 t plots, although the total mass of root dry matter per hectare was the same in both treatments, 3.6 t (Fig. 3). In the most compacted soil (14.5 t) almost no roots had penetrated the soil below 20 cm depth, while in the 4.5 t treatment more than 20% of the total root mass was found between 20 and 50 cm depth. Consequently, root density in the upper soil layers was considerably lower in the less compacted soil. 3.3. Nematode densities After 4 years of grass growth, total numbers of nematodes in the slightly (4.5 t), and in the heavily (14.5 t) compacted soil did not differ significantly throughout the year, and amounted to 123 and 124 ind. per gram fresh soil, respectively (Table 2). However, numbers of bacterivores, herbivores and omnivores/predators were significantly different under both compaction regimes at all sampling dates. The effects of compaction were tested by analysis of variance: numbers of bacterivores in heavily (14.5 t) compacted soil were significantly (p<0.035) lower than in the less (4.5 t) compacted soil, fungivores were not significantly lower in the 14.5 t treatment than in the 4.5 t treatment, herbivores were significantly (p<0.0001) higher in the 14.5 t treatment than in the 4.5 t treatment and finally omnivores/predators were significantly (p<0.0001) lower in the 14.5 t treatment than in the 4.5 t treatment. In the heavily compacted soil the average proportion of the herbivores (almost all Paratylenchus sp.) was ca. 50%, and in the slightly compacted soil 13%. Numbers and proportions of the other feeding types were much higher in the less compacted soil, in particular the omnivores/predators and the bacterivores. With respect to the taxa, herbivorous Paratylenchus sp. were significantly more numerous (3.7×) in the

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Fig. 1. Effects of the various load treatments (0, 4.5, 8.5, 14.5 t) on three physical properties of the grassland soil from 1988 to 1991: (a) thickness (cm) of the initially loosened layer; (b) cone index (MPa) in the 0–5 cm layer; (c) soil moisture content (0/0 ww) in the 0–5 cm layer for the 0 and 14.5 t loads.

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Fig. 2. Effect of various load treatments on above ground dry matter yield of grass for four nitrogen fertilizer rates in 1992.

Table 1 Average annual dry matter yield (kg ha−1 per year) over 1988– 1992, under four load treatments (280 kg N ha−1 per year) Load treatment (t)

Dry matter yield (kg ha−1 )

Index

0 4.5 8.5 14.5

11270 11960 11310 10580

94 100 95 88

heavily compacted soil, while the fungivorous Aphelenchoides sp. was equally abundant in both plots. All other taxa were more numerous in the less compacted soil, with the exception of Panagrolaimus sp., Aphelenchus avenae, Psilenchus sp., and Pratylenchus sp., taxa that only occurred in very small numbers, less than two specimens per gram soil (Table 3).

4. Discussion Passage of load traffic decreased the thickness of the loosened soil layer considerably and already after the first year of the experiment the soil had stabilized into a physical condition where loading and bearing capacity were in equilibrium. Thickness of the loosened layer, bulk density and penetration resistance clearly depended on the load traffic. In all years the 4.5 t loading treatment gave the highest grass yields. Obviously,

a relatively low degree of soil compaction improved physical conditions for crop growth, e.g. created a better root–soil contact (Van Noordwijk and De Willigen, 1984), whereas at higher degrees of compaction roots failed to penetrate deeper soil layers and consequently exploited only the upper 20 cm of soil (Fig. 2b). As a result the optimum for crop yield was observed at the intermediate (4.5 t) treatment. The lower moisture content in the upper soil layers of the less compacted plots may have affected the organisms in that layer, in particular, in summer when moisture contents dropped to ca. 10% (w/w) (Bouwman and Zwart, 1994). However, the nematodes in the dryest plots (4.5 t) were most numerous in June and September, and numbers were even higher than in the 14.5 t treated plots. Consequently, possible negative effects of drought do not seem to have been important. As the moisture contents in the lower soil layers do not significantly differ between differently compacted plots, effects on crop growth are assumed to be insignificant. The number of nematodes 120 g−1 dry soil (∼ =12.106 m−2 0–10 cm ) in the experimental plots investigated is relatively high and the distribution over the feeding types in the less compact soil (4.5 t), with B>F>H>O/P, is common. The strong dominance (50%) of the herbivores in the heavily compacted soil (14.5 t) (H>B>FO/P) is less common, although the dominating herbivorous taxon Paratylenchus is known to peak temporarily or to build up unexpected

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Fig. 3. Effect of two load treatments on cumulative dry matter weight of roots as a function of depth for one nitrogen fertilizer rate (280 kg N ha−1 per year).

Table 2 Abundance of nematodes (feeding groups) in the upper 10 cm of the sod, in numbers per gram dry soil (a) and relative abundance (b), in the 4.5 and 14.5 t load treated plots (280 kg N), at four sampling dates in 1992 Load treatment (a) Numbers 4.5 t

14.5 t

Month

Bacterivores

Fungivores

Omnivores/predators

Herbivores

Totals

March June September December Yab

49a ±17 59±25 70±10 46±18 56±6

25±8 55±17 34±6 39±16 38±8

8±3 20±3 17±4 5±3 13±4

10±5 11±6 33±22 12±2 17±6

93±10 146±31 153±14 102±29 123±17

March June September December YA

45±19 34±10 23±3 29±3 33±5

18±6 14±8 23±6 53±29 27±10

+ 4±2 1±1 3±2 2±1

34±7 62±14 89±4 63±18 62±13

96±11 114±23 136±2 148±48 124±13

53 40 46 45 46

27 38 22 39 31

9 14 11 4 10

11 8 21 12 13

100% – – – –

46 30 17 20 27

19 12 17 36 21

+ 4 1 2 2

35 54 65 42 50

– – – – –

(b) Relative abundance (%) 4.5 t March June September December Yab 14.5 t

a b

March June September December YAb

Means of three replicates ±S.D. Year average.

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Table 3 Average annual abundance’s of nematode taxa in numbers per gram dry soil in the 4.5 and 14.5 t load treated plots in 1992 Nematode taxa

Load treatment 4.5 t

14.5 t

34±4 8±1 7±5 6±2 + +

25±3 3±1 2±1 2±1 0 +

Fungivores Tylenchidae Psilenchidae Aphelenchoides Aphelenchus

28±6 0 10±2 +

14±5 + 12±4 1

Omnivores/predatorsa Dorylaimidae

13±2

2±0

Herbivoresa Paratylenchus Pratylenchus

17±6 0

62±8 +

Bacterivoresa Cephalobidae et al. Monhysteridae et al.a Plectidae Rhabditidae Alaimidae Panagrolaimidae

a

Significantly different numbers in the two plots (p<0.05).

high densities in widely different habitats (Yeates, 1979; Boström and Sohlenius, 1986; Dmowska, 1993). The identified taxa are very common in grasslands, and most of them also in arable soils. Thus, the nematode faunas, developed under the compaction gradient, were not exceptional. The faunistic (feeding guilds) differences between the two investigated plots, however, were most striking. These differences resembled the differences due to soil tillage observed by Parmelee and Aston (1986) and Juma and Mishra (1988) who measured considerably higher densities of bacterivores and lower densities or proportions of herbivores in tilled versus non-tilled plots, while fungivores differed seasonally between the plots but not on an annual basis. Omnivores/predators are often the most sensitive feeding category with respect to tillage, as found by Wasilewska (1979) comparing annual cropping systems with pastures. Comparison of the results of our experiment with the mentioned literature shows that with respect to the feeding guilds the less compact soil resembles the tilled arable plots and the heavily compacted soil resembles the non-tilled plots. It is often mentioned that soil texture, pH, water content, and crop rotation, show the best

correlation with the taxonomic composition of nematode populations (De Goede and Bongers, 1994). The results of our research indicate that soil structure should be added to these parameters, at least with respect to the proportions of the various feeding types. With respect to the shift in structure (feeding guilds, taxa) of the nematode fauna, three aspects have to be considered: (1) The passage of the heavy traffic load causes different levels of direct mortality to the various nematode species (Boag, 1985). A reason for the different vulnerability of species to soil compaction may be that some species occupy structurally more stable niches in the soil then others. As complete equilibrium between load treatment and resilience of the soil was reached within 2 years after the start of the experiment, direct effects may have been strongest during that period. Taxa considered to be vulnerable to direct mechanical damage, e.g. omnivorous Dorylaimidae, equilibrated at lower numbers in the most compacted soil (Table 3). (2) The second aspect in relation to the shifts in the nematode fauna caused by the compaction gradient is that the higher root density in the upper layers of the 14.5 t treated soil indicates an increased amount of feeding sites (∼ = food) for herbivorous Paratylenchus. The increase in numbers of Paratylenchus was not proportional to the increase in root biomass in the 14.5 t treated upper soil layers (+270% versus +25%, as compared to the 4.5 t treatment). However, the total amount of roots is probably not the best parameter to express the amount of feeding sites for ectoparasitic nematodes. The relative increase of fresh young roots could be much higher than the increase in total root mass. Also microbivorous taxa such as Cephalolobidae and Aphelenchoididae can be directly stimulated by root growth and often show increased densities in rhizospheres. It is therefore not unexpected that densities of these taxa did not differ much between the two compaction treatments as they were at the same time stimulated by increased root growth and inhibited by decreased habitable pore space. Root growth not only directly offers food for specific nematode taxa but indirectly also as root-exudates that stimulate microbial growth in pore spaces, not connected with active living roots. Bacterivorous taxa such as Rhabditidae, Plectidae, Monhysteridae, and also omnivorous Dorylaimidae probably are particularly active in such pore spaces, but, despite assumed increased food availability, their

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numbers were considerably lower in the heavily compacted soil than in the slightly compacted soil. This is probably due to the third relevant factor: (3) The decrease of pore space habitable for nematodes, caused by increased soil bulk density. Nematodes living primarily in the soil (macro) pores (Jones and Thomasson, 1976) reacted negatively to the decreased habitable pore space. Bacterivorous Cephalobidae occupy a position in both the rhizosphere and in the soil pores, and their numbers did not differ significantly between the 4.5 and 14.5 t treated plots. It is evident that a certain degree of soil compaction is necessary to obtain optimum crop development and yield. If the soil is too loose (0 t) root contact with the soil particles may be hampered; if it is too compact (8.5 t and 14.5 t), root penetration into the lower soil layers is inhibited. Consequently, exploitation of the soil profile was suboptimal resulting in reduced crop yields The shift in the faunistic composition of the nematodes from microbivorous species associated with decomposition/mineralization processes to herbivorous species associated with crop damage may also explain negative effects on crop yield. Densities of herbivorous Paratylenchus sp. of 30–90 specimens per gram dry soil could be harmful to the grass, as for example, carrots already experience damage at densities of eight specimens per cm3 soil (Weischer, 1959). The total numbers of nematodes not being affected by the degree of soil compaction, indicates that decreased habitable pore space for bacterivores was compensated for by the increased amount of feeding sites for herbivores.

Acknowledgements The authors thank J. Bloem, P.C. de Ruiter and H.G. van Faassen for their help with the manuscript, G. Brouwer for the measurements of root distribution.

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