Vertical Vegetation Structure Below Ground: Scaling from Root

Vertical Vegetation Structure Below Ground:Scaling from Root to GlobeH. Jochen SchenkSo sind wohl manche Sachen, die wir getrost belachen,weil unsre Augen sie nicht sehn.(‘Abendlied’, poem by Matthias Claudius) *1 IntroductionThe structure of vegetation that is below ground truly is the hidden half(Waisel et al. 2002),hidden from view and too often hidden from biologicalresearch. Over the last 30 years,the Biological Abstracts database hasrecorded almost twice as many publications in plant ecology that addressthe ecology of leaves than studies of root ecology. Biologists do not evenhave a term to refer to the subterranean parts of vegetation. In the Englishlanguage,biologists use the term canopy to refer to the collective arrangementof all leaves in a plant community,but lack such a term for roots. (Theold-fashioned word rootage suggests itself.) Despite this unequal attentionto the visible and the hidden halves of vegetation,the two parts are equallyimportant for the function of terrestrial plants and ecosystems and havegeneral functions in common: Both halves are structured to enable resourcecapture. They are made up of organs that are specialized for resourceacquisition,leaves above ground and the distal parts of roots below ground,and of the axes that support and connect these sites of resource acquisitionwithin individual plants. Both also contain structures that are devoted tomechanical support,to storage of resources,and to reproduction; these are,however,beyond the scope of this chapter. Both exhibit a vertical structurethat responds to resources that have a strong vertical dimension,lightabove ground,water, nutrients,and physical soil structure below ground.* Translation: So there are many things,which we scoff at without thought because our eyesdo not see them. (‘Evening song’, poem by Matthias Claudius)Progress in Botany, Vol. 66© Springer-Verlag Berlin Heidelberg 2005

342 EcologyBecause vegetation structure is largely determined by the spatial distributionof resource-acquiring organs,there ought to be predictable relationshipsbetween vertical vegetation structure and the vertical distribution ofplant resources in space and time. Indeed,the structure of plant canopiesis strongly related to the temporal and spatial distribution of light intensity,even though physical factors that act as stressors also play a major role instructuring vegetation above ground (Russell et al. 1989; Ehleringer andField 1993). Understanding such relationships has enabled ecologists to useinformation about environmental conditions to successfully predict thespatial structure of plant canopies at scales ranging from individual plantsto whole communities (Horn 1971; Botkin et al. 1972; Schieving and Poorter1999; Anten and Hirose 2001) and even to global vegetation (Haxeltine andPrentice 1996; Bonan et al. 2003; Sitch et al. 2003).Recent innovations in the methodology of root research (Smit et al. 2000)have enabled much progress toward understanding relationships betweenroots,soil resources,and other physical and biotic soil factors,a factattested to by two recent edited volumes on root biology and ecology(Waisel et al. 2002; de Kroon and Visser 2003). However,until very recentlythere have been relatively few attempts to synthesize and integrate suchinformation in order to develop predictive models of spatial root distributions.Such models are now being developed and are discussed at the endof this chapter.This chapter explores the current state of information about quantitativerelationships between root growth and physical factors,such as soil characteristicsand water availability,and assesses the usefulness of this informationfor developing predictive models of vertical vegetation structurebelow ground at scales ranging from root systems to global vegetation. Suchmodels would greatly help us to quantify interactions between climate,soil,and plants,to better predict patterns of water and nutrient uptake by plants,and thus to better predict changes in the structure and function of vegetationabove and below ground in response to global change. In the following,we will discuss the factors that influence the spatial distribution of roots,beginning at the scale of individual roots and parts of root systems,thenscale up to root systems of individual plants,to plant populations andcommunities,and finally to global vegetation. This is followed by a reviewof theoretical and empirical models that may be used to predict the verticalvegetation structure below ground and scale up from individual roots androot systems to the globe.

Vertical Vegetation Structure Below Ground: Scaling from Root to Globe 3432 Spatial Distribution of Individual Rootsin Response to Soil ConditionsIndividual roots can respond to environmental stimuli by curving,changingelongation rates,growing or abscising branches,or increasing or decreasingroot diameter and specific root length. Together these responsesmake up what is usually referred to as root growth. Other responses toenvironmental factors include changes in root life span (i.e.,root turnover),in root anatomy,or in physiology,and such changes may in turn affect rootgrowth and therefore the architecture of root systems. In the following someexamples of responses that directly affect spatial distributions of roots arehighlighted.2.1 Responses of Root Distributions to Soil StructureThe physical structure of the rooting medium may be more important fordetermining small-scale distributions of roots than any other factor. Rocksin the soil,boundaries between a litter layer and mineral soil,or betweenmineral soil and bedrock will obviously affect root distributions. As strongeffects of tillage on vertical root distributions demonstrate,soil strengthand the distribution and quantity of macropores also greatly affect rootgrowth (Unger and Kaspar 1994; Dwyer et al. 1996; Ball-Coelho et al. 1998).Root elongation rates typically decrease exponentially with increasing soilstrength (Bengough 2003; Bingham and Bengough 2003). The higher thesoil strength of the bulk soil,the more likely are roots to be confined to soilmacropores,such as fissures in clay soils (Dardanelli et al. 2003),animalburrows (Pitkanen and Nuutinen 1997; Springett and Gray 1997),ant nests(Carvalheiro and Nepstad 1996; Moutinho et al. 2003),and root channels(Dell et al. 1983; Gish and Jury 1983; Johnston et al. 1983; van Noordwijk etal. 1991; Rasse and Smucker 1998). In bedrock,roots are always confinedto fissures,where they may play an important role in enlarging rock fissuresand mechanically contributing to weathering (Matthes-Sears and Larson1995; Zwieniecki and Newton 1995; Sternberg et al. 1996; Jackson et al. 1999;Werner and Luepnitz 1999; Hubbert et al. 2001; Witty et al. 2003). Ingeneral,roots strongly respond to the physical structure of the rootingmedium,but they also create and modify physical structure,thus enablingfuture roots to take advantage of such root-mediated soil modifications.

344 Ecology2.2 Root Curvature: Tropic Responses to Environmental StimuliRoots respond to a large variety of environmental stimuli by curving;stimuli include gravity (Knight 1811; Chen et al. 1999),water (Hooker 1915;Takahashi 1994),electrical stimuli (Schrank 1959; Wolverton et al. 2000),temperature (Wortmann 1885; Fortin and Poff 1991),various chemicals(Lilienfeld 1905; Konarzewski and Guminski 1975),oxygen (Porterfield andMusgrave 1998),and mechanical stimuli (Darwin 1880; Ishikawa and Evans1997). Such tropic responses enable roots to grow towards soil regions withfavorable conditions for growth or away from regions with unfavorableconditions. However,the available data suggest that such plastic responsesdiffer greatly between species and depend on the specific combination ofmultiple environmental factors encountered by the roots. Gravitropism isby far the most important of these responses,because it tends to overrideother tropic responses (Takahashi 1994). Gravitropism enables root systemsto direct root growth of main root axes and lateral branches atgenetically determined angles from the vertical,thus increasing the efficiencyat which the soil volume is explored and reducing the probability ofroot overlap within a root system.2.3 Root Proliferation: Local Increases in Root Lengthin Response to Environmental StimuliIn response to resource gradients or resource patches,roots often showproliferation,i.e.,increases in local length density (root length per volumeof soil),either through increased root elongation,increased branching,orboth (Hutchings and de Kroon 1994). Ecological experiments that documentroot proliferation typically do not distinguish between these twoforms of root growth (but see Mou et al. 1997) and simply report measurementsof root length density.2.3.1 Responses of Root Distributions to Soil Water HeterogeneityRoot elongation rates typically are highest at soil water potentials close tothe field capacity of the soil,and decrease linearly or exponentially withdecreasing soil water potential (Teskey and Hinckley 1981; Kuhns et al.1985; Torreano and Morris 1998; Joslin et al. 2001; Zou et al. 2001; Siegel-Issem 2002). This effect is due in part to the increase in soil strength that isassociated with a decrease in water potential (Wraith and Wright 1998). Theminimum water potential at which roots elongate varies greatly between

Vertical Vegetation Structure Below Ground: Scaling from Root to Globe 345species,and is often lower than –1.5 MPa,the limit usually assumed to bethe ‘permanent wilting point’ for plants. Roots of Arabidopsis thalianaseedlings elongated at water potentials of –1.6 MPa in agar (van der Weeleet al. 2000). Roots of various forest tree seedlings also elongate at waterpotentials below –1.5 MPa (Siegel-Issem 2002). Not surprisingly,roots ofdesert plants can elongate at lower soil water potential. Desert succulentsproduced roots at water potentials as low as –2.6 MPa and showed 50% ofmaximum elongation rates at –1.4 MPa (Jordan and Nobel 1984). Roots ofsome desert shrubs elongate at water potentials lower than –6 MPa (Fernandezand Caldwell 1975). Root elongation rates strongly decrease withdecreasing water potentials,but,on average,the limiting water potential islikely to be much lower in dry and seasonally dry environments than inmesic ones.Root proliferation in moist parts of the soil may be caused in part bygrowth towards gradients of increasing relative humidity (Takahashi 1994;Takano et al. 1995; Tsutsumi et al. 2003a,b). Until recently, hydrotropismwas thought to be largely restricted to dry soil where humidity gradientsare steeper than in moist soils (Wraith and Wright 1998). However,recentexperiments designed to decouple hydrotropism from gravitropism suggestthat hydrotropism may be one of the dominant forces shaping rootsystem development (Tsutsumi et al. 2003a).Due to changes in elongation,branching,and hydrotropic growth,verticalroot distributions can change greatly in response to shifts in verticaldistributions of soil water (Wraith and Wright 1998). In response to dryingof the soil surface,root distributions may even change from having thehighest density close to the surface in well-watered soil to having the highestdensity at depth (Klepper et al. 1973). In general,frequent shallow irrigationcauses shallow root distributions and localized drip irrigation causes localroot proliferation around the irrigation source (Fabiao et al. 1990,1995;Meyer and Barrs 1991; Benasher and Silberbush 1992; Carmi et al. 1992,1993). Root responses to soil water heterogeneity tend to be highly plastic(Klepper 1991; Hook and Lauenroth 1994; Tsutsumi et al. 2003a),but onlyif roots can reach moist soil layers without being impeded by dry layers withhigh soil strength (Plaut et al. 1996). Vertical root distributions are mostlikely to shift downward in response to drying when some deep roots arealready present at depth at the onset of the drought (Klepper et al. 1973).2.3.2 Responses of Root Distributions to Soil Nutrient HeterogeneityThere is great variation between plant species in their response to nutrientpatchiness,but on average root length density increases in nutrient-rich

Vertical Vegetation Structure Below Ground: Scaling from Root to Globe 347Fig.2.Soil depth at which maximum lateral root spread was observed for 479 plants ofdifferent growth forms in global,water-limited environments (ratio of mean annual precipitation/meanannual potential evapotranspiration 40% ofall plant-available phosphorus,>30% of total nitrogen,and about 30% ofpotassium (Jobbágy and Jackson 2001). Clearly,nutrient availability isstrongly related to root densities, but on its own does not fully explain thehigh concentration of roots in the upper layers of the soil.

348 EcologyFig. 3. Global average vertical root distribution and 95 percentiles calculated from 564 soilprofiles from many global vegetation types (Schenk and Jackson 2002a). Data are availableonline at http://www.daac.ornl.gov. (Schenk and Jackson 2003a)2.3.3 Responses of Root Distributions to Unfavorable Soil ConditionsShallow rooting depths in boreal,alpine,and tundra vegetation may at leastin part be due to low temperatures of the subsoil (Bonan and Shugart 1989;Kutschera and Lichtenegger 1997). Anaerobic soil conditions (Crawford1992) and soil toxicity,such as high heavy-metal or aluminum concentrations(Baligar et al. 1998) can also restrict root growth,and may be locallyimportant for causing shallow rooting. Vertical root distributions canchange seasonally as soil conditions change (e.g.,Fernandez and Caldwell1975). Roots in soil horizons that develop unfavorable conditions may stopgrowing,may go dormant (Leshem 1970),or die,in some cases due tocontrolled abscission of branches (Pregitzer 2002).2.4 Effects of Roots on the Soil Environment:Potential Feedbacks into Spatial PatternsSoil formation and development is greatly affected by plants, especially byroots and their associated microbial organisms (Jenny 1980). Roots andtheir rhizoflora modify their soil environment by altering its structure,

Vertical Vegetation Structure Below Ground: Scaling from Root to Globe 349texture,carbon content,water contents,nutrient contents,pH,and byadding organic root exudates and organic matter,as well as by the effectsof all of these factors on microbial communities and the soil fauna. Russianecologists have called such plant-generated soil alterations phytogenicfields when they are associated with individual plants (Uranov 1965; Kryshen2000). More generally,one may refer to such phenomena as phytogenicsoil modifications. Little research has been done to address the effectsof phytogenic modifications on resulting spatial patterns in root distributions.They could potentially result either in positive feedbacks if rootspersist or even proliferate in soil space modified by roots,or in negativefeedbacks if roots avoid or grow poorly in such modified soil space.Examples of negative feedback effects in roots are well documented formany annual crops. A lack of crop rotation often leads to poor root growth,usually due to an accumulation of soil pathogens (Olsson and Alstrom1996). This negative feedback effect tends to be species-specific and mayincrease species diversity by increasing species turnover during succession(Mills and Bever 1998). Root-mediated allelopathy is another example ofsuch species-specific negative feedback effects (Schenk et al. 1999; Bais etal. 2003). Vertical root distributions will be affected by negative feedback ifdifferent species replacing each other differ markedly in their root distributions,butthe quantitative significance of such effects for the persistenceand dynamics of vertical vegetation structure below ground is unclear.More important for the development of the vertical vegetation structurebelow ground are probably positive feedback effects,which promote theproliferation of roots where roots had been previously established. I havealready mentioned that roots often grow in macropores created by otherroots that may still be alive or may have been decomposed. Furthermore,roots may ameliorate the soil through exudates and components of mucilagewhich increase the availability of inorganic nutrients (Inderjit 2003;Read et al. 2003),affect mineral weathering (Bormann et al. 1998),andcreate and stabilize soil aggregates (Graham et al. 1995). Roots can alsoredistribute water in the soil environment and transport it into dry parts ofsoils,thereby enabling roots to extend into soil horizons that may not oftenbe reached by infiltration or may rapidly dry due to surface evaporation(Hunter and Kelley 1946; Schulze et al. 1998; Burgess et al. 2001). Water mayalso reach dry parts of the soil due to gravitational flow along existing rootsand root channels (Johnston et al. 1983; Karpachevskiy et al. 1995; Whitfordet al. 1995; Martinez-Meza and Whitford 1996; Devitt and Smith 2002).Hydraulic redistribution and preferential water flow along roots can rapidlyrecharge deep soil layers (Burgess et al. 2001; Ryel et al. 2003) and mayaccount for the occurrence of deep roots in habitats where water infiltrationis typically shallow. Redistribution of water in the soil allows roots to

350 Ecologymaintain a relatively stable distribution in the soil rather than constantlyshifting distributions with every change in soil water status.Effects of roots on soil fertility may involve both positive and negativefeedback. Roots and their associated microorganisms and soil fauna are themain source for soil nitrogen,which means that soils previously occupiedby roots contain more nitrogen than those that never contained roots.However,roots also locally deplete nutrients,which may temporarily inhibitfurther root growth in the depletion zones. In the long term,plantactivities redistribute nutrients in the soil profile by locally reducing concentrationsof those nutrients that are typically most limiting to growth,nitrogen,phosphorus,and potassium,and by adding nutrients to surfacelayers via litterfall (Jobbágy and Jackson 2001). In some cases,root activitiescan drastically and rapidly change soil nutrient status and pH,as has beenobserved for Eucalyptus trees planted in the Argentinean Pampas (Jobbágyand Jackson 2003).In general,negative feedback effects are likely to largely affect individualspecies and thus species composition,while positive feedback effects willenable roots of many species to grow in soil previously occupied by roots.Such positive feedback effects may even persist after disturbances and affectthe rooting patterns of successional vegetation. Where deep roots occurredbefore a major disturbance removed much of the vegetation,the subsequentsuccessional vegetation may grow roots down existing root channelsand thus quickly reestablish deep roots (Sommer et al. 2000, 2003).3 Spatial Structure of Root Systems of Individual PlantsThe architecture of individual root systems can be analyzed quantitativelyby topological analysis of branching patterns (Fitter et al. 1991; Smilauerovaand Smilauer 2002; Robinson et al. 2003). This approach can beused to characterize the efficiency of root systems in exploring soil space,to quantitatively compare root systems,and to quantify the phenotypicplasticity of root growth (Fitter and Stickland 1991,1992). Analyses of rootsystem architecture and branching angles have also been used to determinethe degree of competition within an individual root system (Ge et al. 2000).Recent findings suggest that individual roots encountering another rootmay be able to distinguish whether that root belongs to the same plant ora different plant and alter growth patterns accordingly (Mahall and Callaway1991,1992; de Kroon et al. 2003; Falik et al. 2003; Holzapfel and Alpert2003). The ability to discriminate between self and non-self roots couldpotentially decrease intra-plant competition.

Vertical Vegetation Structure Below Ground: Scaling from Root to Globe 351Many other studies that address variables structuring root systems ofindividual species could be mentioned here,but reviewing such studieswould be of limited value in the context of this chapter because the speciesis not a useful unit for scaling up from individuals to communities andbiomes. Theoretically,phylogeny may play a role in structuring communities,butthere is currently a lack of evidence to support such a role (Silvertownet al. 2001),and therefore no way to scale up from species-specifictraits to properties of communities or ecosystems (Naeem and Wright2003). Of course,if one had data on typical morphologies and sizes of rootsystems for all plant species within a given region one could probably usethis information to predict vertical root distributions at the plant communitylevel. Such detailed information on multiple species is actually available,butonly for very few regions. Over the last century a handful ofresearchers have excavated hundreds of root systems and documented theirmorphologies in detailed drawings,for example John Weaver in the NorthAmerican Midwest (1919,1920),M.S. Shalyt in the Ukraine and inKazakhstan (1950,1952),Isa Baitulin in Kazakhstan and Mongolia (1979,1993),and Lore Kutschera,Erwin Lichtenegger,and colleagues in centralEurope (many volumes,from Kutschera 1960 to Kutschera and Lichtenegger2002). The importance of this ground- and backbreaking work for ourunderstanding of the variability of root system morphology and speciesspecificdifferences can hardly be overstated. However,in order to use thismassive amount of information for predictions at the community level itfirst has to be converted into quantitative data.Scanned drawings of root systems have been used to quantify rootsystem sizes and shapes (Sun et al. 1997) and to analyze differences betweenroot systems of different plant growth forms and quantify relationshipsbetween root system sizes,climate,and soil characteristics (Schenk andJackson 2002b),as well as for analyses of plant allometry (Casper et al.2003). Strong allometric relationships exist between the volumes occupiedby individual plant canopies and the volumes occupied by their root systems,andthese relationships span taxonomically and ecologically diversespecies across ten orders of magnitude of size (Karl J. Niklas,H.J. Schenk,and R.B. Jackson,unpubl. data). Variance in aboveground sizes statisticallyaccounts for a large proportion of the variance in root system sizes betweenplant growth forms (Fig. 4; Schenk and Jackson 2002b). As a case in point,no differences in rooting depths or lateral root spreads were found in ananalysis of large numbers of species of perennial grasses and perennialforbs,two growth forms that typically differ substantially in above- andbelowground plant architecture,but have similar size ranges (Schenk andJackson 2002b). These growth forms may differ in the architecture of rootsinvolved in anchorage,but the volume of a root system is defined by the

352 EcologyFig.4.Relationship between plant height and maximum rooting depth for seven plantgrowth forms in global,water-limited environments (ratio of mean annual precipitation/meanannual potential evapotranspiration

Vertical Vegetation Structure Below Ground: Scaling from Root to Globe 353Fig.5.Schematic diagram of the relationship between mean annual precipitation (MAP)and plant rooting depths. The drawings of individual plants approximate the medianrooting depths for three broad growth form categories along the MAP gradient. Themaximum rooting depths depicted were those for 95% of all plants in the respectiveprecipitation range,i.e.,only 5% of plants in that growth form category had deeper rootsthan indicated by these lines. Also shown are the changing plant density and changingproportions of annual herbs,perennial herbs,and semi-shrubs/shrubs along the gradient,from deserts and shrublands dominated by woody plants to grasslands dominated byherbaceous plants. (Schenk and Jackson 2002b, reproduced with permission)by phreatophytic trees in arid lands,which tend to be the most deeplyrooted plants on Earth (Table 1).4 Spatial Structure of Root Systems in Plant Populationsand CommunitiesStudies of root system architecture in soil typically involve plants growingin monospecific stands or in more or less diverse plant communities,whichmeans that these root systems are grown in competition with roots fromother plants. Studies on root systems of single plants in the absence ofcompetition are typically done in pots,and observations from such studiesmay be difficult to extrapolate to natural settings. Until quite recently,fewstudies had addressed the effects of root competition on spatial root distributions.In a review of such studies,Fitter (1987) found little evidence forsignificant effects of root competition on spatial root distributions. Suchevidence began to accumulate in the 1990s,beginning with a seminal studyby Mahall and Callaway (1991) on roots of two desert shrub species, Larreatridentata and Ambrosia dumosa. Root elongation rates of both specieswere found to significantly decrease when roots encountered Larrea roots,

354 EcologyTable 1. Plant rooting depths greater than 30 m that have been reported in the scientific literature. Other accounts of deep roots exist,but mostof these are anecdotal. The world record for deepest roots according to the Guinness Book of Records (2003) is said to be about 120 m for a figtree (Ficus sp.) near Ohrigstad,South AfricaSpecies Maximum Geographic location Climate Sourcerooting depth(m)Acacia erioloba 45 Kalahari,Botswana Arid Leistner (1967)Acacia erioloba 60 Kalahari,Botswana Arid Jennings (1974)Acacia tortilis ssp. raddiana 35 Niger Arid Fagg (1991)Boscia albitrunca 68 Kalahari,Botswana Arid Jennings (1974)Eucalyptus calophylla 36.5 SW Australia Humid Campion (1926)Eucalyptus marginata 40 S Western Australia Humid Dell et al. (1983)Faidherbia albida 40 SW Niger Semi-arid Leduc et al. (2001)Juniperus monosperma 61 New Mexico,USA Arid Cannon (1960)Prosopis juliflora 35 Sahel region Arid Breman and Kessler (1995)Prosopis velutina 58 Arizona,USA Arid Phillips (1963)Prosopis cineraria 60 Oman Arid Brown (1992)

Vertical Vegetation Structure Below Ground: Scaling from Root to Globe 355and,for Ambrosia,also when its roots encountered other Ambrosia roots.Several studies published since 1991 have addressed the effects of rootcompetition on spatial root distributions,and their results have beenreviewed extensively by Schenk et al. (1999),de Kroon et al. (2003),andHutchings and John (2003). To briefly summarize the findings to date: (1)root growth in many species reacts to the presence of other roots; (2) in atleast some cases such reactions are triggered by signals between roots or byallelochemicals; (3) types of reactions differ depending on the speciesinvolved; and (4) reactions appear to be different when roots encounterroots from the same plant or from a separate plant. The overall ecologicaleffects of these mechanisms seem to be that they allow plants to shift rootgrowth to soil space unoccupied by roots,or,if such space is unavailable,to soil space occupied by roots of competitors,and to reduce intra-plantroot overlap.The overall effect at the community level of shifts in root distributionsin response to competition is that soil space is partitioned more efficientlyby roots than it would be without these mechanisms. For example,verticalroot distributions of some species may shift in response to interspecific rootcompetition and thus exhibit vertical niche partitioning (D’Antonio andMahall 1991; Mou et al. 1997; Leuschner et al. 2001; Schmid and Kazda2001). Niche partitioning by multiple species has been found to increaseresource use efficiency at the community level and thereby increase primaryproductivity (Loreau and Hector 2001). Partitioning of the soil spaceby roots of multiple species is likely to be complex and the patterns will bespecies-specific. It should not be assumed that different plant growth formsor functional types tend to partition the soil profile in a similar fashion indifferent ecosystems. For example,Heinrich Walter’s (1939) classic twolayerhypothesis of soil depth partitioning between woody and herbaceousplants,originally proposed for African savannas,does not appear to beuniversally applicable and may be largely restricted to relatively dry climates(Fig. 5; Schenk and Jackson 2002b).Regardless of whether root growth reacts to the presence of other roots,all terrestrial plant species have evolved under conditions of root competitionand are therefore likely to have evolved a root system architecture androot growth patterns that allow them to grow and survive in the presenceof competitors. As mentioned above,roots tend to proliferate in nutrientrichpatches of the soil,even though such proliferation may not in itselfincrease nutrient uptake rates. Instead it confers advantages by pre-emptingor reducing the use of such patches by competitors (Robinson et al.1999; Robinson 2001). The effect of such root proliferation in fertile patchesor soil layers will be that,within a soil profile,root densities will increasemore than linearly with nutrient concentrations. This may in part explain

356 Ecologythe observations discussed above that the upper 0.2 m of soil profilescontains on average > 40% of all plant-available phosphorus (Jobbágy andJackson 2001) but almost 60% of all roots (Fig. 3).Because most soil profiles receive most of their water inputs from above,the upper soil layers will be most likely to contain plant-available water(except the surface layer which is directly affected by soil evaporation).Root competition will favor placement of roots into those soil layers thathave the most reliable access to water,and shallow roots will generallyconfer competitive advantages over deeper roots in soils that receive mostwater by infiltration from above (van Wijk and Bouten 2001).Because of the diversity of root system architectures in diverse plantcommunities,niche partitioning,and competition,vertical root distributionsin communities are more likely to be closely associated with thedistribution of soil resources than the root distributions of individualplants or mono-specific stands. The overall effect of plant diversity onvegetation structure is that it decreases the proportion of variance explainedby phylogenetic components and thus increases the proportionexplained by environmental variance,including the ecological history ofthe community (e.g.,successional status) and environmental factors. Thereduction of the phylogenetic component means that spatial communitystructure can be predicted, at least to some degree, if its history andenvironmental variables are known.5 Belowground Spatial Structure of Global VegetationMaximum plant rooting depths and vertical root distributions for globalbiomes were first compiled and analyzed by Robert B. Jackson and coworkers(Canadell et al. 1996; Jackson et al. 1996). Schenk and Jackson(2002a,b, 2003a) further expanded these data sets, analyzed relationshipsof rooting depths with climate,soil texture,and vegetation types,and usedthese analyses to develop models and maps of global plant rooting depths(Schenk and Jackson 2003b; Schenk and Jackson 2004). Three variableswere used to characterize vertical root distributions: the soil depth abovewhich 50% of all roots are located (D 50 ),the depth above which 95% of allroots are located (D 95 ),and,for individual plants,the maximum rootingdepth (D max ). Globally, D 50 was less or equal to 0.3 m and D 95 was less orequal to 2 m for 90% of all soil profiles. Deeper rooting depths were mainlyfound in seasonally water-limited ecosystems and in warm-temperate totropical environments (Schenk and Jackson 2002a). Climatic variablesmost strongly and positively correlated with rooting depths were annualpotential evapotranspiration (PET) and precipitation. Globally,the domi-

Vertical Vegetation Structure Below Ground: Scaling from Root to Globe 357nant plant growth forms and soil texture explained only minor proportionsof the total variance in rooting depths. Responding to the need for rootparameters for global climate models,Schenk and Jackson (2003b) developedglobal maps of average rooting depths using nonlinear regressionmodels relating D 50 and D 95 to PET, precipitation, and vegetation type.Predicting average rooting depths is problematic and associated withsubstantial errors because of the enormous spatial variability of verticalroot distributions. In recognition of this problem,Schenk and Jackson(2004) developed global maps of the probability of deep rooting (ratherthan mean rooting depths) based on two global data sets of rooting depths,long-term means of monthly precipitation,and potential evapotranspiration,andsoil texture (Figs. 6 and 7). According to these analyses,deep roots(defined as D 95 > 2 m) are most likely to occur in seasonally dry,semi-aridto humid tropical regions under savanna or thorn-scrub vegetation orunder seasonally dry semi-deciduous to evergreen forests. Deep roots areFig.6.Global probability of deep rooting (defined as > 5% of all roots below 2 m) as afunction of mean annual precipitation and mean annual potential evapotranspiration(PET). Area shaded in different tones of gray represents the regional climatic averages ofterrestrial 0.5° latitudinal-longitudinal grid cells for the late 20th century. Climates in thewhite part of the graph did not globally exist during this period,at least not as grid cellaverages. The climatic continuum is divided into humidity zones according to UNEP (1992).Probabilities of deep rooting were calculated from the empirical distribution of records fordeep roots within the climatic continuum,using an analysis described in Schenk andJackson (2004)

358 EcologyFig. 7. Global distribution of the predicted probability of deep rooting (defined as > 5% ofall roots below 2 m) for 1° latitudinal-longitudinal grid cells,calculated by a non-linearregression model relating the probability of deep rooting to precipitation,potential evapotranspiration,andsoil texture. (Modified from a figure in Schenk and Jackson 2004)least likely to occur in arctic,boreal,or cool-temperate regions and inper-humid climates such as equatorial rainforests. Under warm-temperateto tropical climates,rooting depths are more likely to be deep in coarse-texturedand fine-textured soil than in soils of medium texture. These mapsare the first empirically based maps of global rooting depths,but they arebased on limited data,so systematic sampling will be required to test thesepredictions for areas for which no root data are available.6 Scaling from Root to Globe: Predictive ModelsA large number of variables affect root growth and vertical root distributions(see summary in Table 2). If the responses of root growth and rootdemography to all these variables could be incorporated into a mathematicalmodel,then such a model could theoretically be used to predict verticalvegetation structure below ground for individual plants,plant communities,orglobal biomes. No single mathematical model published to dateincorporates all of the variables listed in Table 2 explicitly,but several

Vertical Vegetation Structure Below Ground: Scaling from Root to Globe 359Table 2. Important variables to be considered in the development of models used forpredicting belowground structure of vegetation at the scale of plant communities to globalbiomes. Predictions for individual plants or plant populations may require considerationof additional variables,such as species-specific root system architecture. Depending on thespatial and temporal scale of the model,not all of these variables will have to be modeledexplicitly, and/or additional variables may have to be included. See text for further discussionsof all variables listedGeneral categories Specific variables Potential effects on rootsMechanical soil 1. Vertical distribution 1. With increasing soil strength rootproperties of soil strength growth declines,and roots areincreasingly likely to preferentiallygrow in soil macropores2. Vertical distribution 2. Affects the relationship between soilof soil texture,water potential and soil waterincluding rockscontent and thereby root growth3. Vertical distribution 3. Affects presence and abundanceof soil structure of macropores which can affectpatterns of root growth andinfiltrationChemical soil 1. Vertical distribution 1. Affects soil water holding capacityproperties of organic matter and fertility. Roots typicallyproliferate in soil that is rich inorganic matter2. Vertical distribution 2. Roots proliferate in soil volumesof plant-available with high contents of plant-availablenutrientsnitrogen and phosphorus3. Vertical distribution 3. Toxins may negatively affectof toxins,especially root growthaluminum concentrationsSoil water balance1. Inputs: precipitation,1. Affect infiltration depth,run-on,groundwater vertical distribution of soil watercontents, and thereby root growth2. Outputs: runoff and 2. Affect vertical distribution of soilevapotranspiration water contents and thereby rootgrowth3. Vertical distribution 3. Affects water flow rates,rootof hydraulicwater uptake,and potentiallyconductivityhydrotropic root growth4. Dynamic vertical 4. Affects vertical distribution of rootdistribution of soil growth,including due towater resultinghydrotropismfrom 1—3

360 EcologyTable 2. ContinuedGeneral categories Specific variables Potential effects on rootsBiotic variables 1. Plant sizes above 1. Root system sizes are positivelygroundcorrelated with shoot system sizes2. Costs (construction,2. Root distributions generally (butmaintenance) and not always) will reflect efficient usebenefits (resource of energy (carbon) and nutrientsuptake) of root growth by plants3. Root competition 3. Shifts root distributions to parts ofthe profile with higher resourceavailability (water and nutrients)4. ‘Permanent wilting 4. The lowest soil water potential forpoints’ of root growth root growth is lower for plants indry environments than in wetenvironmentsPhytogenic soil 1. Positive feedback 1. Root-mediated soil modificationsmodifications effects allow roots to grow more easilywhere previous roots have grownbefore2. Negative feedback 2. ‘Lack of crop rotation’ effects.effectsRoots may ‘avoid’ strong overlapwith roots from the same plant.Some species have root systems thatexclude other roots throughallelochemicalsprocess-based models have been developed in recent years that incorporateat least some of the more important variables required to predict verticalroot distributions. Following Wraith and Wright (1998),modeling approachesmay be divided into models of root system architecture,whichsimulate root branching patterns,and continuum models that calculateroot mass or root length density for given locations in the soil.6.1 Models of Root System ArchitectureRecent models used to calculate effects of nutrient distributions on threedimensionalroot distributions include those by Somma et al. (1998) andDunbabin et al. (2002). The latter also incorporates effects of soil strengthand water content on root growth. Ge et al. (2000) modeled three-dimen-

Vertical Vegetation Structure Below Ground: Scaling from Root to Globe 361sional root growth in response to heterogeneous distributions of phosphorusin the soil and also analyzed the effects of different branching patternson competition among roots of the same plant. Ho et al. (2004) addedresponses to heterogeneous distributions of soil water to this model. Rootdistributions resulting from hydrotropic growth were simulated successfullyin two dimensions by a model developed by Tsutsumi et al. (2003a,b).In two other recent modeling studies (Grant 1998; Biondini 2001),simulationsof three-dimensional root growth were incorporated into highlycomplex plant growth models that simulate numerous aspects of plantgrowth,development, and resource allocation in response to environmentalconditions. Root growth in these models responds to heterogeneousdistributions of nutrients and soil water.6.1.1 Continuum Models of Root GrowthRecent two-dimensional continuum models that incorporate responses ofroot densities to soil conditions include the model of Chen and Lieth (1993),in which root densities respond to soil water potential and temperature,and the model of Heinen et al. (2003),in which roots respond to nutrientcontents. In the one-dimensional models of Adiku et al. (1996) and vanWijk and Bouten (2001),root densities respond to soil water content. Bothof these models simulate vertical root distributions using optimizationmethods. Such methods are discussed below. Continuum models holdpromise for application at the community level,where explicit simulationsof the root system architectures of multiple plants would be impractical.6.1.2 Optimization Approaches to Predict Vertical Root DistributionsOptimization schemes that distribute vertical root distributions in waysthat minimize plant energy expenditure and/or maximize water and nutrientuptake have been used in several models,at scales ranging from the levelof individual root systems (Ge et al. 2000; Ho et al. 2004) to the globe(Kleidon and Heimann 1998). The continuum model by Adiku et al. (1996)used an optimization scheme to partition roots within the soil profile inorder to maximize water uptake while minimizing plant energy use. Arelated approach was used in a model developed by van Wijk and Bouten(2001),in which roots were distributed vertically so as to maximize wateruptake in the presence or absence of root competition. In a model bySchwinning and Ehleringer (2001) a carbon-gain optimization scheme wasused to partition roots of different functional types of desert plants between

362 Ecologytwo soil layers in response to fluctuating rainfall regimes. Kleidon andHeimann (1998) used a global biosphere model to predict optimized rootingdepths that would maximize net primary production (NPP). Rootingdepth in that model was represented by the depth of a soil compartmentcomprised of a single soil layer.Optimization approaches hold promise for application at all hierarchicallevels ranging from the individual to communities and the biosphere,butgreat care has to be taken when choosing variables for optimization,becausethese variables will differ substantially depending on the hierarchicalscale. For example,high resource use efficiency or high productivity ofplant species may be favored by natural selection under some circumstances(e.g.,Dudley 1996),but wasteful resource use that pre-empts competitorsfrom accessing resources may actually be favored in competitiveenvironments (Cohen 1970; DeLucia and Schlesinger 1991; Gersani et al.2001). Highly productive species are not necessarily better competitorsthan plants of low productivity (Loreau and Hector 2001). Thus speciesshould not be expected to maximize resource use efficiency or productivity.‘Optimal’ root growth traits for individual species are those that maximizefitness in a given environment,including its competitive regime,and predictingsuch traits for individual species in specific places may be of littlehelp in understanding community structure in general.Plant communities are more likely to optimize resource use efficiencythan individual species,because community structure responds to environmentalfactors by changing species composition in addition to the processesof phenotypic plasticity,gene–environment interactions,and naturalselection operating at the species level. Species composition matters greatlyfor ecosystem function at the local scale (Lavorel and Garnier 2002), but itcan change over time and allow additional species to take advantage ofresources not used by previously established species. On average,suchchanges over time would tend to increase resource-use efficiency at thecommunity level. NPP of plant communities tends to increase linearly withthe supply of both solar energy and water (Rosenzweig 1968; Chong et al.1993),and this would not be the case if resource-use efficiencies at thecommunity level fluctuated widely and randomly. Recent studies of theeffects of biodiversity on NPP suggest that,on average,plant interactionsand resulting niche partitioning in diverse communities tend to increaseresource use efficiency at the community level (Loreau and Hector 2001)and thus shift NPP towards the optimum level that can be achieved giventhe physical constraints of the environment and the phylogenetic constraintsof the species in the community,which is not to suggest that theoptimum level is ever attained.

Vertical Vegetation Structure Below Ground: Scaling from Root to Globe 363Based on this line of reasoning,it may be postulated that vertical rootdistributions of communities will tend to approach shapes that maximizewater and nutrient use efficiency at the community scale. This developmentwill be driven by plastic root growth in response to environmental conditions,positiveand negative species interactions,the resulting niche partitioningof the soil profile,successional changes in species composition,andby positive feedback effects. One may further predict that root distributionsafter major disturbances and in early successional or species-poor communitiesare less likely to approach optimal resource use efficiency and aremore likely to be restricted to shallow soil layers which usually offer thegreatest amount of resources at the lowest cost to plants (Gale and Grigal1987).These ideas about resource use optimization at the community levelwere the basis for a conceptual model of global rooting depths (Schenk andJackson 2002b),which was based on the observation that many of thevariables shaping vertical root distributions (see Table 2) tend to favorshallow roots over deep roots: (1) energy costs for construction,maintenance,andresource uptake are lower for shallow roots; (2) water in mostsoils enters the profile predominantly from above; (3) nutrient concentrationsare typically highest in the upper soil layers; (4) shallow soil layers areusually less likely to be oxygen-deficient; and (5), because of reasons(1)–(4),shallow roots generally have competitive advantages over deeperroots. Based on this conceptual model,rooting depths should only increaseif (1) there is transpirational demand for water that cannot be fulfilled bytaking up water stored closer to the soil surface and (2) water is available atdepth. Therefore,average rooting depths are predicted to be shallow in coldenvironments due to low transpirational demand,shallow in dry environmentsregardless of the thermal regime because of a general lack of waterat depth,shallow in per-humid environments because deep roots are notneeded there to fulfill transpirational demands,and deep in warm andseasonally dry environments because of high transpirational demands andthe availability of deep soil water. Analyses of large data sets of rootingdepths from dry environments (Schenk and Jackson 2002b) and from abroad range of global environments (Schenk and Jackson 2004) stronglysupport these general trends (Fig. 6),thereby allowing the predictions forthe global distribution of deep roots depicted in Fig. 7. Much furtherresearch will be required to test the validity of the assumptions underlyingthe conceptual model of Schenk and Jackson (2002b),to test the accuracyof the global map in Fig. 7,and to develop process-based mathematicalmodels that can increase the accuracy of predictions.

364 Ecology7 Conclusions and Future ChallengesRoots experience a resource environment that has a strong vertical dimension.Just as leaves respond to the vertical distribution of light in a canopy,roots will respond to vertical gradients of nutrients,water,and other soilproperties. Just as the top of the canopy is generally the optimal locationfor leaves,so the upper soil layers are the optimal location for roots. Someplants do not compete for the best spot in the canopy; they are shadeadaptedand specialized to live at the lower edge of the canopy. Similarly,some plants will be adapted to be deeply rooted and will not compete withother species for the abundant resources in upper soil layers. However,unlike the top of the canopy which may be out of reach for any but the tallestspecies,the upper soil layers are reachable by all plants,and thereforevertical stratification of the soil profile by different species is less likely tobe as pronounced as vertical stratification of the canopy.Roots live in a heterogeneous and complex environment,but,as thischapter shows,their average responses to soil conditions are predictable toa large degree. Moreover,roots modify the soil environment,and thepositive feedback effects of root-mediated soil modifications make rootdistributions more stable and predictable than they would be without sucheffects.Root research faces many methodological challenges,but it now hasaccess to a large variety of tools and methods (Smit et al. 2000). Over recentdecades,it has moved from description to explanation and,by takingadvantage of descriptive work accumulated over many decades,is now wellon its way towards prediction. Because of the large number of variablesaffecting root growth,our predictions about root behavior will never bevery precise,but the increasing number of ecological models that successfullypredict general patterns of root distributions demonstrates that ourunderstanding of root ecology has greatly progressed in recent years.Obviously,being able to predict root distributions is still a long way fromunderstanding the spatial distribution of root function. We are only beginningto understand the functional diversity of roots within root systems(Pregitzer 2002). There is mounting evidence that water and nutrient uptakefrom a soil volume are not always closely related to root length densityor root surface area within that volume (Adiku et al. 2000; Robinson 2001),proving that roots,just like leaves,are not all alike and are capable ofadjusting their physiologies in response to external or internal signals(Forde and Lorenzo 2001; Pregitzer 2002). Root dormancy is another neglectedissue that will have large effects on the distribution of functionswithin root systems (North and Nobel 1998). Studies of root functionrequire a different set of tools from root distribution studies,such as tracers

Vertical Vegetation Structure Below Ground: Scaling from Root to Globe 365of nutrient and water uptake (Casper et al. 2003) and inverse modelingapproaches that calculate root function from changes in the distribution ofsoil resources (Adiku et al. 2000; Hupet et al. 2003). The greatest challengein root research remain mycorrhizae and their effects on root distributionand function. The vertical distribution of mycorrhizal hyphae below theupper soil layers is an open research question for most terrestrial ecosystems(Rosling et al. 2003).Ecologists cannot be accused to ever ‘scoff at what their eyes cannot see’– to paraphrase the German poet Matthias Claudius – but too often in thepast have they ignored what their eyes did not see. Too often the soilremains the black box of studies in terrestrial ecology (Hammer 1998). Thevisible and hidden halves of plants,of vegetation,and of ecosystems deserveand need equal attention.Acknowledgements. The author wishes to thank Susan Schwinning and David Robinson forhelpful comments on the manuscript and Laura Middlebrooke for help with data processing.This research was made possible in part by a postdoctoral fellowship from the NationalCenter for Ecological Analysis and Synthesis [a Center funded by NSF (DEB-94-21535),theUniversity of California at Santa Barbara,and the State of California] and by a grant fromthe Andrew W. Mellon Foundation.ReferencesAdiku SGK,Braddock RD,Rose CW (1996) Modelling the effect of varying soil water on rootgrowth dynamics of annual crops. Plant Soil 185:125–135Adiku SGK, Rose CW, Braddock RD, Ozier-Lafontaine H (2000) On the simulation of rootwater extraction: examination of a minimum energy hypothesis. Soil Sci 165:226–236Anten NPR,Hirose T (2001) Limitations on photosynthesis of competing individuals instands and the consequences for canopy structure. Oecologia 129:186–196Bais HP,Vepachedu R,Gilroy S,Callaway RM,Vivanco JM (2003) Allelopathy and exoticplant invasion: from molecules and genes to species interactions. Science 301:1377–1380Baitulin IO (1979) Kornevaja sistema rastenij aridnoj zony Kazakhstana (in Russian). (Rootsystems of plants of the arid zone of Kazakhstan) Nauka, Alma-AtaBaitulin IO (ed) (1993) Fitoékologicheskie issledovanija v juzhnoj Gobi (in Russian withEnglish summary). (Phytoecological investigations in southern Gobi) Gylim,Alma-AtaBaligar VC,Fageria NK,Elrashidi MA (1998) Toxicity and nutrient constraints on rootgrowth. HortScience 33:960–965Ball-Coelho BR, Roy RC, Swanton CJ (1998) Tillage alters corn root distribution in coarsetexturedsoil. Soil Till Res 45:237–249Benasher J,Silberbush M (1992) Root distribution under trickle irrigation – factors affectingdistribution and comparison among methods of determination. J Plant Nutr 15:783–794Bengough AG (2003) Root growth and function in relation to soil structure,composition,and strength. In: de Kroon H,Visser EJW (eds) Root ecology,vol 168. Springer,BerlinHeidelberg New York,pp 151–171Bingham IJ,Bengough AG (2003) Morphological plasticity of wheat and barley roots inresponse to spatial variation in soil strength. Plant Soil 250:273–282Biondini M (2001) A three-dimensional spatial model for plant competition in an heterogeneoussoil environment. Ecol Model 142:189–225

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Vertical Vegetation Structure Below Ground: Scaling from Root to Globe 373Zwieniecki MA,Newton M (1995) Roots growing in rock fissures: their morphologicaladaptations. Plant Soil 172:181–187H. Jochen SchenkDepartment of Biological ScienceCalifornia State University FullertonP.O. Box 6850Fullerton,California 92834-6850,USATel.: +1-714-2783678Fax: +1-714-2783426e-mail: jschenk@fullerton.edu