Effects of plant roots on soilpreferentialpathways and soilmatrix in forest ecosystems

Effects of plant roots on soilpreferentialpathways and soilmatrix in forest ecosystems

Yinghu Zhang•Jianzhi Niu•Weili Zhu•Xiaoqing Du•Jiao Li

To characterize effects of plant roots on preferential flow(PF),we measured root length density(RLD) and root biomass(RB)in Jiufeng National Forest Park, Beijing,China.Comparisons were made for RLD and RB between soil preferential pathways and soil matrices.RLD and RB declined with the increasing soil depth(0–10, 10–20,20–30,30–40,40–50,50–60 cm)in all experimentalplots.RLD was greater in soilpreferentialpathways than in the surrounding soil matrix and was 69.5,75.0 and 72.2%for plant roots of diameter(d)＜1,1＜d＜3 and 3＜d＜5 mm,respectively.Fine root systems had the most pivotal influence on soil preferential flow in this forestecosystem.In allexperimentalplots,RB contentwas the sum of RB from soil preferential pathways and the soil matrix in each soil depth.With respect to 6 soil depth gradient(0–10,10–20,20–30,30–40,40–50,50–60 cm)in each plot,the number of soil depth gradient that RB content was greater in soil preferential pathways than in the soil matrix was characterized,and the proportion was 68.2%in all plots.

Preferential flow·Preferential pathways· Soil matrix·Root length density·Root biomass

Introduction

Studies of plant roots with respect to edaphology and plant hydrological responses have been hampered by difficulties associated with mechanisms of water movementand solute transport,especially preferential flow(Bundt et al.2001). Preferential flow describes preferential channels for water movement and solute transport from soils to roots.Pores formed by plant roots play an important role in hydrologicalresponses.Studies of the functions of plantroots began in the early eighteenth century and gradually increased in number.Plant roots play a pivotal role in water uptake, nutrients acquisition,solute retention and soilconservation during plant growth.Plant roots grow into soil pores to form continuous channels for water and nutrient uptake (Tracy et al.2011).The relationships between plant roots and soil preferential flow were described by Aber et al. (1985),Steudle(1994),Stokes et al.(2009),and Ceccon et al.(2011).Li and Ghodrati(1994)used breakthrough curve methods to demonstrate the effects of channels formed by plant roots on preferential transport of nitrates. Price and Hendrick(1998)found that root biomass(RB) varied by season and that living root length density(RLD) was greatest in autumn while dead RLD was greatest in winter.Volkmar(1993)confirmed that RLD had no absolute correlation with soil bulk density.Jørgensen et al. (2002)reported that soil profiles containing root channels enhanced solute transportand water movement to a greater extent than soilprofiles without root channels.Dusˇek et al. (2006)reported that plant root zones led to more water movement.Bogner et al.(2010)used stained patterns to determine that RLD reflected preferential flow extent and that RLD was larger in preferential pathways than in the soil matrix.Both living and decayed roots provide preferred paths for soil water and solute transport(Tippku¨tter1983;Angers and Caron 1998),and there is an important relationship between living and decayed roots.Bottner et al.(1999)demonstrated that living roots had effects on soil carbon metabolism during decayed root decomposition.Compared with decayed roots,living roots released more dissolved organic carbon(DOC)(Hsieh and Yang 1992)and this accelerated decomposition of dead roots. However,decayed roots prompted more water movement than living roots(Mitchell et al.1995).Edwards et al. (1988)demonstrated that the proportion of decayed root channels of diameter＜1 mm was 80%per m2in soil preferential pathways.

There are increased interests in evaluating plant roots of forest ecosystems because of their role in regulating the cycling of water and nutrients for plants growth,but plant roots are difficult to measure in any forest ecosystems (Cairns et al.1997).The upper diameter limit of fine roots varies among differentstudies and ranges from 1 to 5 mm. Following the original studies,data are available for two diameter limits:roots＜2 mm and roots＜5 mm(Kurz etal. 1996).Tufekcioglu et al.(1999)reported that fine and small roots(＜5 mm)and coarse roots(＞5 mm)are two major components of plant roots,and their vertical distributions modified soil physical and biological properties. Meanwhile,they sorted roots into diameter classes of 0–2 mm(fine root)and 2–5 mm(small root).Vanninen and Ma¨kela¨(1999)classified fine root compartments as: small fine roots(diameter 0–2 mm),large fine roots (diameter 2–5 mm)and total fine roots(diameter 0–5 mm). Fine roots’share of total biomass rarely represents more than 5%of total biomass of trees(Lo´pez et al.2001), while Santantonio et al.(1977)and Fogel(1983)reported that coarse and fine roots as a proportion of total tree biomass varied between 18 and 45%.Brassard et al. (2011)stated that coarse root biomass(diameter＞1 mm) could account for approximately 30%of total biomass in forestecosystems.Maybe fine plantroots has been found to vary above in relation to forest stand characteristics,i.e. tree species,stand age,density,basal area and soil properties,or environmental factors,chiefly air temperature, amount of precipitation,geographical location and elevation(Vogt et al.1996;Jackson et al.1997;Leuschner and Hertel 2003).Jackson et al.(1997)estimated fine root biomass and reported that live fine root biomass ranged from 130 g m-2in deserts to 950 g m-2in temperate grasslands.

Many studies of the relation of plantroots to preferential flow have been conducted in farmland ecosystems to characterize the effects of soil compaction,tillage systems and management on preferential flow.Few studies concentrated on forest soils that contain more plant roots and stones.Noguchi et al.(1997)reported that at least 70%of the macropores(＞2 mm)in topsoil and 55%in subsoil in forest soils were associated with plantroots.Hagedorn and Bundt(2002)showed that preferential flow paths in a structured forest soil persisted for decades.Beven and Germann(1982)observed that macropores formed by forest tree roots could persist for at least 50–100 years. Studies on preferential flow in forest ecosystems,especially stony lands,are few.In these systems,soil matrix flow and preferential flow are pivotal flow patterns influencing water and solute transport.In forest ecosystems, channels formed by plant roots can contribute to physical non-equilibrium at the individual plot scale(Jarvis et al. 2012).Our study aimed to determine if plant roots have greater biomass and/or occur in greater density in preferential pathways than in the soil matrix.We conducted field dye tracing experiments in a forest ecosystem in Jiufeng National Forest Park,Beijing,China,using the food dye Brilliant Blue FCF(Colour Index 42090)to trace preferential flow(stained areas)and soil matrix flow(unstained areas)(Hagedorn and Bundt2002).Jiufeng National Forest Park is an important water conservation area which influences the groundwater security of Beijing.The objectives of our study were to:(1)compare RLD and RB of roots of diameter＜1,1–3,and 3–5 mm between preferential pathways and the soilmatrix;and(2)determine which root diameter class contributes most to preferential flow.

Materials and methods

Study area

Our study was a forest ecosystem in Jiufeng National Forest Park(116°28′E,39°34′N),Beijing,China.Jiufeng National Forest Park is part of Beijing Forestry University and is used for teaching and scientific research.Elevation ranges from 60 to 1,100 m a.s.l.The climate is temperate continental with mean annual precipitation of 630 mm, mean annual temperature 11.6°C,and mean annual potential evapo-transpiration of 19,000 mm.The dominant vegetation at elevations＜800 m a.s.l.was plantation of Platycladas orientalis,Pinus tabulaeformis,Quercus spp., Robinia pserdoacacia containing shrubs Prunus armniaca and Vitex chinensis.Above 800 m a.s.l.,P.tabulaeformis, Popular chinensis,Lespedeza bicolon,Spiraca trilobata, Caragana rosea dominated the sparse forest cover.The soil has been described as sandy loam containing approximately 30%rock fragments and gravels(Li et al.2013).

Experimental treatment

In July 2012,we established six experimentalplots within a 10×10 m quadrat situated in representative vegetation at 260 m a.s.l.Plots 1 and 2 were located in Sophorajaponica,plots 3 and 4 in P.orientalis,and plots 5 and 6 in Quercus dentata sections of the quadrat.Preferential flow was identified by monitoring the movement of coloured solution added to each plot.Brilliant Blue FCF dye solution(5 g L-1)was applied to the experimentalplots during the growth season.The solution was uniformly applied to a 1.2×1.2 m area centered on the experimental trees to avoid border effects(Hagedorn and Bundt 2002;Legout et al.2009).Horizontal and vertical soil profiles were excavated when the solution had infiltrated the soil(Hu et al.2013).Horizontal profiles were extracted from 0.5×0.5 m quadrats and vertical profiles with maximum dying depth were extracted from points centered on the experimental trees one day after dye tracer application (Hagedorn and Bundt2002).For the horizontaland vertical sections,soil cores were extracted from preferential pathways and the soil matrix.Preferential pathways were identified by stained areas and soil matrices by unstained areas(Hagedorn and Bundt 2002).We used a camera to record preferential pathway distributions(Fig.1).

Root parameters

RLD and RB are pivotal indices of water and solute transport in forest ecosystems,especially of preferential flow.Soil-free roots were dried for 48 h in an oven at 70°C to constant weight(Castellanos et al.2001;Helmisaari et al.2007)and then weighed using an electronic balance(DV215CD(81 g/0.01 mg))to obtain plant roots. RB(g m-2)(Makkonen and Helmisaari 2001)was usually measured by oven drying(Livesley etal.1999).Fine RB is calculated on the basis of the cross-sectional area of soil cores.RLD(totalrootlength per soilvolume)(Mosaddeghi et al.2009;Glab 2013)was measured using WinRHIZO (STD4800)(Himmelbauer et al.2004;Yan et al.2011).

Fig.1 Identification of preferential pathways and soil matrix from stained areas and unstained areas by applying Brilliant Blue solution. The flow patterns show the stained flow paths in black:stained areas as preferential pathways and unstained areas as soil matrix.Part A was used as a horizontal profile and part B as a vertical profile

Root sampling

Each plot was excavated from horizontal cross sections in 10 cm depth increments 24 h after application of Brilliant Blue FCF dye solution.Undisturbed soil samples were taken at each depth using soil corers(7 cm diameter, 5 cm height,200 cm3volume)with two replications in preferential pathways and the soil matrix.Samples were taken to a depth of 60 cm(0–10,10–20,20–30,30–40, 40–50,50–60 cm)in all experimental plots.Soil cores were stored at-2°C(Castellanos et al.2001)and soil was separated from roots using 5 mm sieves.When necessary,samples were placed in dishes with 4–5 mm deep water so that roots spread and soil particles could easily be removed(Castellanos et al.2001;Yan et al. 2011).We defined fine root diameter as≤5 mm,as commonly used in other studies(Kurz et al.1996;Fine´r et al.2011).

Root contribution to preferential flow

The contribution of plant roots to preferential flow represented an index evaluating which kinds of root diameter functions the largest positively.Firstly,all plantroots from preferentialpathways in each plotwere described,and total sum of plant roots in preferential pathways obtained. Afterwards,the contribution of plant roots to preferential flow was monitored:total sum of plantroots in preferential pathways divided by plant roots d＜1,1＜d＜3, 3＜d＜5 mm,respectively.

Root general comparison

General comparison(GC)evaluated in this paper represented an index determining the difference of plant roots content between preferential pathways and the soil matrix. On the basis of the index,it is not complex to discriminate which one of plantroots contentwas greater in preferential pathways and the soil matrix.The simplified equation will be given as follows:

whereηis GC(%),αPPis plantroots contentin preferential pathways,αSMis plant roots content in the soil matrix.In general,willbe applied to whenαPPis smaller thanαSM,while whenαPPis larger thanαSM,will be applied to.

Fig.2 Proportion of RLD by three classes of root diameter(d＜1,1–3,3–5 mm)in preferential pathways and in the soil matrix in six plots, Sophora japonica Linn for plots 1 and 2,Platycladus orientalis Franco for plots 3 and 4,Quercus dentata Thunb for plots 5 and 6

Statistical analysis

One-way ANOVA was used to assess differences in mean RLD and RB between preferential pathways and the soil matrix and to characterize the effects of root parameters on preferential flow.Data were analzyed using SPSS software.

Results

RLD in preferential pathways and the soil matrix

Differences in RLD by root diameter class(＜1,1–3 and 3–5 mm)in six experimental plots containing three types of vegetation are shown in Fig.2.On the whole,RLDdeclined with increasing soil depth for all three root diameter classes.RLD from soil preferential pathways and the soil matrix in each soil depth also showed a similar tendency.From Fig.2,greatest RLD was recorded in the upper soil layers to a depth 30 cm(topsoil).Meanwhile, plantroots of diameter＜1 mm were mostly distributed on the soil surface.With respect to all experimental plots, RLD content for plant roots of diameter(d)＜1,1＜d＜3 and 3＜d＜5 mm was also the sum of RLD from soil preferentialpathways and the soilmatrix in each soildepth. For 6 soil depth gradient(0–10,10–20,20–30,30–40, 40–50,50–60 cm)in each plot,the number of soil depth gradient that RLD content for plant roots of diameter (d)＜1,1＜d＜3 and 3＜d＜5 mm was greater in soil preferential pathways than in the soil matrix was quantified.The characterizing results were illustrated in Table 1. The proportion of RLD in preferential pathways was greater than in the soil matrix in 69.5%of plots for roots of diameter＜1 mm,in 75%of plots for roots of diameter 1–3 mm,and in 72.2%of plots for roots of diameter 3–5 mm.As shown in Fig.2 and Table 2,roots of diameter＜1 mm were the predominant component for preferential flow in all experimental plots.Roots of diameter＜1 mm accounted for almost 95.0%of preferential flow.

Table 1 The proportion of the number of soil depth gradients(0–10, 10–20,20–30,30–40,40–50,50–60 cm)where RLD content was greater in soil preferential pathways than in the soil matrix among those 6 soil depth gradients(0–10,10–20,20–30,30–40,40–50, 50–60 cm)in each experimental plot

Table 2 Root contribution to preferential flow in all experimental plots

RB in preferential pathways and the soil matrix

RB of fine roots(d＜5 mm)was densely concentrated in the upper soil layers and varied by forest type.On the whole,RB declined with increasing soil depth whether in soilpreferentialpathways or in the soilmatrix(Table 3).In allexperimental plots,RB contentwas the sum of RB from soil preferential pathways and the soil matrix in each soil depth.With respectto six soildepth gradient(0–10,10–20, 20–30,30–40,40–50,50–60 cm)in each plot,the number of soil depth gradient that RB content was greater in soil preferential pathways than in the soil matrix was characterized,and the proportion was 68.2%in all plots.The difference of plant roots content(e.g.,RB,d＜5 mm) between preferential pathways and the soil matrix was illustrated in Fig.3.From Table 3,22 surveyed data of RB from soil preferential pathways and the soil matrix in all experimental plots were characterized.And GC was also calculated by means of Eq.(1).Average GC was 83% calculated from 22 surveyed data.As it was shown in Fig.3,shaded circles represented that root general comparison of RB was higher than 83%;and the other open circles are below 83%.From Fig.3,the number of shaded circles whose root general comparison of RB higher than 83%was thirteen,while the number of open circles was nine.Those surveyed data whose GC was above 83% accounted for 59.1%among 22 surveyed data.However,it was ambivalent when GC was below 83%.From Fig.3, we implied that there were nine surveyed data whose GC was below 83%.

Discussion

In our results,on the whole,plant roots(e.g.,root length density and root biomass)declined with increasing soil depth whether in preferential pathways and in the soil matrix.These results were in agreementwith Himmelbauer et al.(2010)and Bengough(2012).Meanwhile,greatest plant roots were recorded in the upper soil layer to a depth of 30 cm(topsoil).This result was similar to that reported by Lipiec et al.(2003)and Bonger et al.(2008,2010).

Our results also confirmed thatplantroots in preferential pathways were higher than in the soil matrix to some extent,particularly those distributed in the upper soil layers,because plant roots there were mostly decayed or decaying to form more preferential channels.During root decomposition,more channels are formed along the root surface.Preferential pathways provide pores or cracks and this encourages rootgrowth.The surrounding soilmatrix is too compacted for rootgrowth.Meanwhile,our results also implied thatmore and more fine plantroots were located on the soilsurface.This resultsupports the findings of Raizadaet al.(2013).With respect to fine plant roots in this paper, its growth cycle is shorter than coarse plantroots.Thus fine plant roots will become decaying even decayed roots gradually.During the process,plant roots will decompose more organic matters to form more root channels.

Table 3 Root biomass(g m-2) in preferential pathways and the soil matrix by soil depth(0–10, 10–20,20–30,30–40,40–50, 50–60 cm)

Fig.3 Root general comparison of RB in all experimental plots. Shaded circles representthatrootgeneralcomparison of RB is higher than 83%;and the other open circles is below 83%

Preferential pathways in forest ecosystems include higher organic carbon content and microbial biomass compared with soil matrix(Backna¨s et al.2012).By accumulating soil organic matters and redistributing nutrients in the soil profile,preferential pathways play significantrole in their surrounding environments,particularly the soil matrix(Persson 2000).Our field experiments were carried outduring heavy rain,soilwater flow in preferential pathways and cracks increases,and fine roots may become asphyxiated even die.Clusters of fine roots are sometimes observed along or atthe end of coarse roots and correspond to zones of major organic nutrients and water uptake.Fine roots have high decay and emission rates,and clusters may soak up water during rainy season and may contribute to decayed flow paths(Ghestem et al.2011).

Conclusions

RLD and RB declined with increasing depth of soil.Roots were concentrated in topsoil(0–30 cm).RLD and RB were greater in topsoil than in deeper soils.Roots of diameter＜1 mm accounted for the greatest proportion of all roots. RLD and RB were larger in soil preferential pathways than in the soil matrix.The contribution to preferential flow of roots of diameter＜1 mm was greatest.

AcknowledgmentsWe thank the Key Laboratory Soil and Water Conservation and Desertification Combating,Ministry of Education, China for laboratory assistance.

Aber JD,Melillo JM,Nadelhoffer KJ,McClaugherty CA,Paster J (1985)Fine root turnover in forest ecosystems in relation to quantity and form of nitrogen availability:a comparison of two methods.Oecologia(Berlin)66:317–321

Angers DA,Caron J(1998)Plant-induced changes in soil structure: processes and feedbacks.Biogeochemistry 42:55–72

Backna¨s S,Laine-Kaulio H,Kløve B(2012)Phosphorus forms and related soil chemistry in preferential flow paths and the soil matrix of a forested podzolic till soil profile.Geoderma 189–190:50–64

Bengough AG(2012)Water dynamics of the root zone:rhizosphere biophysics and its control on soil hydrology.Vadose Zone J 11(2),doi:10.2136/vzj2011.0111

Beven K,Germann P(1982)Macropores and water flow in soils. Water Resour Res 18:1311–1325

Bogner C,Wolf B,Schlather M,Huwe B(2008)Analysing flow patterns from dye tracer experiments in a forest soil using extreme value statistics.Eur J Soil Sci 59:103–113

Bogner C,Gaul D,Kolb A,Schmiedinger I,Huwe B(2010) Investigating flow mechanisms in a forest soil by mixed-effects modeling.Eur J Soil Sci 61:1079–1090

Bottner P,Pansu M,Sallih Z(1999)Modelling the effect of active roots on soilorganic matter turnover.Plant Soil216:15–25

Brassard BW,Chen HYH,Bergeron Y,Pare D(2011)Coarse root biomass allometric equations for Abies balsamea,Picea mariana,Pinus banksiana,and Populus tremuloides in the boreal forest of Ontario,Canada.Biomass Bioenergy 35:4189–4196

Bundt M,Widmer F,Pesaro M,Zeyer J,Blaser P(2001)Preferential flow paths:biological‘hotspots’in soils.Soil Biol Biochem 33(6):729–738

Cairns MA,Brown S,Helmer EH,Baumgardner GA(1997)Root biomass allocation in the world’s upland forests.Oecologia 111:1–11

Castellanos J,Jaramillo VJ,Sanford RL Jr,Kauffman JB(2001) Slash-and-burn effects on fine rootbiomass and productivity in a tropical dry forestin Me´xico.For Ecol Manag 148:41–50

Ceccon C,Panzacchi P,Scandellari F,PrandiL,Ventura M,Russo B, Millard P,Tagliavini M(2011)Spatial and temporal effects of soil temperature and moisture and the relation to fine rootdensity on rootand soilrespiration in a mature apple orchard.Plant Soil 342:195–206

Dusˇek J,Vogel T,Lichner L,Dohnal M,´A(2006)Simulated cadmium transport in macroporous soil during heavy rainstorm using dual-permeability approach.Biologia 61:S251–S254

Edwards WM,Norton LD,Redmond CE(1988)Characterizing macropores thataffectinfiltration into nontilled soil.Soil Sci Soc Am J 52:483–487

Fine´r L,Ohashi M,Noguchi K,Hirano Y(2011)Fine rootproduction and turnover in forest ecosystems in relation to stand and environmental characteristics.For Ecol Manag 262:2008–2023

Fogel R(1983)Root turnover and productivity of coniferous forest. Plant Soil71:75–85

Ghestem M,Sidle RC,Stokes A(2011)The influence of plant root systems on subsurface flow:implications for slope stability. Bioscience 61:869–879

Glab T(2013)Impact of soil compaction on root development and yield of meadow-grass.Int Agrophys 27:7–13

Hagedorn F,Bundt M(2002)The age of preferential flow paths. Geoderma 108:119–132

Helmisaari HS,Derome J,No¨jd P,Kukkola M(2007)Fine root biomass in relation to site and stand characteristics in Norway spruce and Scots pine stands.Tree Physiol 27:1493–1504

Himmelbauer ML,Loiskandl W,Kastanek F(2004)Estimating length,average diameter and surface area of roots using two different image analyses systems.Plant Soil 260:111–120

Himmelbauer ML,Loiskandl W,Rousseva S(2010)Spatial root distribution and water uotake of maize grown on field with subsoil compaction.J Hydrol Hydromech 58:163–174

Hsieh YP,Yang CH(1992)A method for quantifying living roots of Spartina(Cordgrass)and Juncus(Needlerush).Estuaries Coasts 15(3):414–419

Hu B,Han CL,Jia Y,Zhao ZH,Li FM,Siddique KHM(2013) Visualization ofthethree-dimensionalwater-flowpathsin calcareous soilusing iodide watertracer.Geoderma 200–201:85–89

Jackson RB,Mooney HA,Schulze ED(1997)A global budget for fine root biomass,surface area and nutrient contents.Proc Natl Acad Sci USA 94:7362–7366

Jarvis NJ,Moeys J,Koestel J,Hollis JM(2012)Preferentialflow in a pedological perspective.Hydropedology,75–120

Jørgensen PR,Hoffmann M,Kistrup JP,Bryde C,Bossi R,Villholth KG(2002)Preferentialflow and pesticide transportin a clay-rich till:field,laboratory,and modeling analysis.Water Resour Res 38:1246–1261

Kurz WA,Beukema SJ,Apps MJ(1996)Estimation of root biomass and dynamics for the carbon budget model of the Canadian forest sector.Can J For Res 26:1973–1979

Legout A,Nys C,Picard JF,Turpault MP,Dambrine E(2009)Effects of storm lothar(1999)on the chemicalo composition of soil solution and on herbaceous cover,humus and soils(Fougeres, France).For Ecol Mang 257:800–810

Leuschner C,Hertel D(2003)Fine root biomass of temperate forests in relation to soil acidity and fertility,climate,age and species. Prog Bot 64:405–438

Li YM,Ghodrati M(1994)Preferential transport of nitrate through soil columns containing root channels.Soil Sci Soc Am J 58(3):653–659

LiX,Niu JZ,Xie BY(2013)Study on hydrologicalfunctions oflitter layers in North China.PLoS One 8(7):e70328.doi:10.1371/ journal.pone.0070328

Lipiec J,Medvedev VV,Birkas M,Dumitru E,Lyndina TE, Rousseva S,Fulajtar E(2003)Effect of soilcompaction on root growth and crop yield in Central and Eastern Europe.Int Agrophys 17:61–69

Livesley SJ,Stacey CL,Gregory PJ,Buresh RJ(1999)Sieve size effects on root length and biomass measurements of maize(Zea mays)and Grevillea robusta.Plant Soil 207:183–193

Lo´pez B,Sabate´S,Gracia CA(2001)Annual and seasonal changes in fine root biomass of a Quercus ilex L.forest.Plant Soil 230:125–134

Makkonen K,HelmisaariHS(2001)Fine rootbiomassand production in Scots pine stands in relation to stand age.Tree Physiol 21:193–198

Mitchell AR,Ellsworth TR,Meek BD(1995)Effectof root systems on preferential flow in swelling soil.Commun Soil Sci Plant Anal 26:2655–2666

Mosaddeghi MR,Mahboubi AA,Safadoust A(2009)Short-term effects of tillage and manure on some soil physical properties and maize rootgrowth in a sandy loam soilin western Iran.Soil Tillage Res 104:173–179

Noguchi S,Tsuboyama Y,Sidle RC,Hosoda I(1997)Spatially distributed morphologicalcharacteristics of macropores in forest soils of Hitachi Ohta Experimental Watershed,Japan.J For Res 2:207–215

Persson H(2000)Adaptive tactics and characteristics of tree fine roots.Dev Plant Soil Sci 33:337–346

Price JS,Hendrick RL(1998)Fine root length production,mortality and standing root crop dynamics in an intensively managed sweetgum(Liquidambar styraciflua L.)coppice.Plant Soil 205:193–201

Raizada A,Jayaprakash J,Rathore AC,Tomar JMS(2013)Distribution of fine rootbiomass of fruitand forest tree species raised on old river bed lands in the north west Himalaya.Trop Ecol 54(2):251–261

Santantonio D,Hermann RK,Overton WS(1977)Root biomass studies in forest ecosystems.Pedobiologia 17:1–31

Steudle E(1994)Water transport across roots.Plant Soil 167:79–90

Stokes A,Atger C,Bengough AG,Fourcaud T,Sidle RC(2009) Desirable plant root traits for protecting natural and engineered slopes against landslides.Plant Soil 324:1–30

Tippku¨tter R(1983)Morphology,spatial arrangement and origin of macropores in some Hapludalfs,West Germany.Geoderma 29: 355–371

Tracy SR,Black CR,Roberts JA,Mooney SJ(2011)Soilcompaction: a review of past and present techniques for investigating effects on root growth.J Sci Food Agric 91:1528–1537

Tufekcioglu A,Raich JW,Isenhart TM,Schultz RC(1999)Fine root dynamics,coarse root biomass,root distribution,and soil respiration in a multispecies riparian buffer in Central Iowa, USA.Agrofor Syst 44:163–174

Vanninen P,Ma¨kela¨A(1999)Fine rootbiomass of Scots pine stands differing in age and soil fertility in southern Finland.Tree Physiol 19:823–830

Vogt KA,Vogt DJ,Palaiotto PA,Boon P,J,Asbjornsen H (1996)Review ofrootdynamics in forestecosystems grouped by climate,climatic forest type and species.Plant Soil187:159–219

Volkmar KM(1993)A comparison of minirhizotron techniques for estimating root length density in soils of different bulk density. Plant Soil157:239–245

Yan HF,Li K,Ding H,Liao CS,Li XX,Yuan LX,Li CJ(2011)Root morphological and proteomic responses to growth restriction in maize plants supplied with sufficient N.J Plant Physiol 168:1067–1075

23 January 2013/Accepted:19 October 2013/Published online:30 January 2015

ⒸNortheast Forestry University and Springer-Verlag Berlin Heidelberg 2015

Project funding:This research was supported by a grant from the Natural Science Foundation of China(41271044).

The online version is available at http://www.link.springer.com

Corresponding editor:Hu Yanbo

Y.Zhang·J.Niu(✉)·W.Zhu·X.Du·J.Li

Key Laboratory Soiland Water Conservation and Desertification Combating,Ministry of Education,College of Soil and Water Conservation,Beijing Forestry University,Beijing 100083, China e-mail:nexk@bjfu.edu.cn