Underground Processes 2003

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SPECIAL FEATURE

Underground Processes in Plant Communities1

This set of papers represents the second Special Feature this year offering new insights into

interactions in the rhizosphere. From a historical perspective, early ecologists saw the need and

importance of underground research. Nearly 25% of the classic plant ecology textbook by John

Weaver and Frederic Clements (1929. Plant Ecology. McGraw-Hill, New York, New York, USA)

was devoted to soil, roots, and their interactions with other organisms. Although most modern

ecologists recognize the important role of underground processes, they find the rhizosphere dif-

ficult to study, with the organisms ranging in size from tiny (microbes) to gigantic (roots).

Unfortunately, out of sight usually means out of mind, and strong programs linking the rhizosphere

to plant community processes are few and far between. The fact that more than half of the plant

biomass in grasslands is underground is not reflected in the types of studies most commonly

conducted. The bulk of this underground biomass is involved in various symbioses, antagonistic

assaults, and mutualisms. For example, fungal root pathogens form some of the largest knownliving organisms and are extensively studied by applied and mechanistic biologists but are rather

infrequently the focus of ecological studies. The authors of this Special Feature make strong

arguments for a prominent role of underground dynamics in driving competitive processes between

plants, interactions between plants and animals, and community and ecosystem level processes

such as succession and nutrient cycling. This set of papers represents a fresh combination of

conceptual and empirical approaches that matches the state-of-the-art in ecological research.

The opening papers (Bargett and Wardle, van der Putten) introduce the concept of aboveground

belowground linkages in plant communities and apply well developed ideas on plantanimal

interactions from aboveground to underground processes. For example, although little ecological

research has been conducted on the manifold defensive strategies of roots, it is quite likely that

roots employ both direct defense by producing toxins and indirect defense by attracting enemies

of root herbivores. Root exudates may cause beneficial microbes to flourish and nourish plants

in times of aboveground defoliation. The authors pose a novel mixture of potential interactions

that have consequences extending from physiological to ecosystem ecology. Following the twointroductory papers, the Special Feature next focuses on the role of microbes in community

processes (Reynolds et al., Klironomos).

Although a single milliliter of soil can contain over 100 million individuals of bacteria and

other microbes, their specificity in interactions, functional roles, and consequences have been

little explored. Mycorrhizal fungi are robbing some plants and feeding others, and we are only

beginning to scratch the surface in determining what factors influence the continuum of parasitic

to mutualistic interactions. This gets more and more complicated as we begin to see that some

mycorrhizae can act as conduits allowing for the flow of resources between roots of taxonomically

distant plants. Of course, the circle of life is not completed until the roots themselves are recycled,

and mycorrhizal fungi may play an important role here as well (Langley and Hungate). Indeed,

microbes are simultaneously feeding, infecting, and recycling the phyto-ecosystem.

The latter part of the Special Feature focuses on plantplant interactions underground and how

these may scale up to community and ecosystem processes. Casper et al. mine data from a large

database and merge this with experimental results and a model that helps us define the rootneighborhood that may ultimately determine plantplant competition. In addition to the proximity

and overlap in roots underground, the foraging and proliferation of roots in heterogeneous soils

may determine the levels of competition between plants at the individual level and also may have

consequences for populations and communities (Hutchings et al.).

1 Feature accepted 31 October 2002. Reprints of this 79-page Special Feature are available for $12.00 each,either as pdf files or as hard copy. Prepayment is required. Order reprints from the Ecological Society of America,Attention: Reprint Department, 1707 H Street, Suite 400, Washington, D.C. 20006.


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Rhizo-ecologists have already been successful in unraveling some of the poorly understood

complexities of real communities. The authors of the papers in this Special Feature have now

challenged ecologists to come to further grips with how a variety of both aboveground and

belowground organisms, from arthropods and microbes to interacting plants themselves, interact

via the rhizosphere. Although these processes will remain out of sight, they will increasingly be

studied and revealed.

ANURAG AGRAWAL

Special Features Editor

Key words: belowground competition; community dynamics and succession; multi-trophic interactions;mycorrhizae; plant defense and herbivory; soil and nutrient heterogeneity.

2003 by the Ecological Society of America


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Ecology , 84(9), 2003, pp. 22582268 2003 by the Ecological Society of America

HERBIVORE-MEDIATED LINKAGES BETWEEN ABOVEGROUND ANDBELOWGROUND COMMUNITIES

RICHARD D. BARDGETT1,4 AND DAVID A. WARDLE2,3

1Institute of Environmental and Natural Sciences, Lancaster University, Lancaster, LA1 4YQ UK2Landcare Research, P.O. Box 69, Lincoln, New Zealand

3Department of Forest Vegetation Ecology, Swedish University of Agricultural Sciences, SE901-83 Umea, Sweden

Abstract. Understanding how terrestrial ecosystems function requires a combinedabovegroundbelowground approach, because of the importance of feedbacks that occurbetween herbivores, producers, and the decomposer subsystem. In this paper, we identifyseveral mechanisms by which herbivores can indirectly affect decomposer organisms andsoil processes through altering the quantity and quality of resources entering the soil. Weshow that these mechanisms are broadly similar in nature for both foliar and root herbivory,regardless of whether they operate in the short term as a result of physiological responsesof individual plants to herbivore attack or long-term following alteration of plant communitystructure by herbivores and subsequent changes in the quality of litter inputs to soil. Wepropose that a variety of possible mechanisms is responsible for the idiosyncratic natureof herbivore effects on soil biota and ecosystem function; positive, negative, or neutral

effects of herbivory are possible depending upon the balance of these different mechanisms.However, we predict that positive effects of herbivory on soil biota and soil processes aremost common in ecosystems of high soil fertility and high consumption rates, whereasnegative effects are most common in unproductive ecosystems with low consumption rates.The significance of multiple-species herbivore communities is also emphasized, and wepropose that if resource use complementarity among herbivore species or functional groupsleads to greater total consumption of phytomass, and thus greater net herbivory, then bothpositive and negative consequences of increasing herbivore diversity for belowground prop-erties and processes are theoretically possible. Research priorities are highlighted and in-clude a need for comparative studies of herbivore impacts on above- and belowgroundprocesses across ecosystems of varying productivity, as well as a need for experimentaltesting of the influence of antiherbivore defense compounds on complex multitrophic in-teractions in the rhizosphere and the significance of multiple herbivore species communitieson these plantsoil interactions.

Key words: decomposition; ecosystem function; herbivores; multitrophic interactions; nutrient

mineralization; plant litter; root herbivores; soil biota; soil fauna.

INTRODUCTION

It is increasingly becoming recognized that to un-

derstand how terrestrial ecosystems function requires

a combined abovegroundbelowground approach, be-

cause of the importance of feedbacks that occur be-

tween the producer and the decomposer subsystems

(Van der Putten et al. 2001, Wardle 2002). These feed-

backs between plants and decomposer organisms in-

volve a variety of interactions, but they are also strong-

ly influenced by herbivores that consume plant material

(Bardgett et al. 1998b). Many studies on impacts of

herbivores on terrestrial ecosystems have focused ex-clusively on aboveground responses, such as changes

in vegetation diversity and community structure (e.g.,

Collins et al. 1998). Further, there is currently evidence

that herbivores have substantial indirect effects on soil

Manuscript received 3 May 2002; revised 20 July 2002; ac-cepted 11 September 2002; final version received 7 October2002. Corresponding Editor: A. A. Agrawal. For reprints of thisSpecial Feature, see footnote 1, p. 2256.

4 E-mail: [email protected]

organisms and their activities including soil minerali-

zation processes, and this may be expected to have

significant consequences for plant productivity and

community structure (Bardgett et al. 1998b). Recent

studies also show that root herbivores can exert sub-

stantial indirect effects on soil biota and cycling of

nutrients, with important aboveground effects (Bard-

gett et al. 1999a, b, Denton et al. 1999). However, much

remains unknown about the roles of root herbivores in

regulating soil biological properties, but as with foliar

herbivores, their effects on soil biota and processes

appear to be related to qualitative and quantitativechanges in resource supply to soil resulting from their

consumption of plant material.

Here we evaluate how both foliar and root herbivory

may influence belowground organisms and processes,

and how these changes in soil biological properties may

in turn affect aboveground primary production. In do-

ing this, we explore the different mechanisms for such

effects over various temporal and spatial scales, rang-

ing from the individual plant to the plant community.


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Given that several types of herbivores may be simul-

taneously operating in the same plant community, we

then discuss and make predictions on the issue of be-

lowground effects of herbivory in the context of mul-

tiple herbivore species communities. The ultimate goal

of this article is to predict the main ways that herbivores

affect soil biota and processes, and ultimately the func-tioning of terrestrial ecosystems, and identify some fu-

ture research questions that are central to furthering

our understanding in this field.

PRODUCERDECOMPOSER FEEDBACK MECHANISMS

Very little is known about the precise way that soil

organisms and processes are affected by foliar and root

herbivory. This is because of the existence of a wide

variety of mechanisms that operate at both the indi-

vidual plant and the plant community scale, which can

involve either positive or negative effects on both the

quantity and quality of resources that enter the decom-

poser subsystem (Bardgett et al. 1998b). Consistent

with this variety of effects, studies that have usedfenced exclosure plots to investigate the ecological

consequences of grazing and browsing by mammals

have found overall effects on decomposer organisms

that can be positive (e.g., Stark et al. 2000, Bardgett

et al. 2001) or negative (e.g., Suominen 1999), effects

on C mineralization that are positive (e.g., Bardgett et

al. 1997, Kielland et al. 1997) or negative (e.g., Pastor

et al. 1988, Stark et al. 2000), and effects on net N

mineralization that are positive (e.g., McNaughton et

al. 1997a, Frank and Groffman 1998) or negative (e.g.,

McNaughton et al. 1988, Stark et al. 2000; reviewed

in Wardle 2002). Further, in a study of 30 long-term

(1336-yr-old) fenced plots aimed at excluding intro-

duced deer and goats in a range of New Zealand rainforests, Wardle et al. (2001) showed that effects on soil

biota, C mineralization, and C and N sequestration were

highly idiosyncratic, with roughly equal numbers of

sites showing strong positive and strong negative ef-

fects. There are no comparable studies looking at the

effects of excluding root herbivores on soil biological

properties at the field scale, but we predict that the

variety of feeding strategies of root-feeding organisms

and the wide range of responses of plants to infestation

will yield equally idiosyncratic responses at the eco-

system level.

Despite the existence of the wide variety of ways

that herbivores can influence producerdecomposer

feedbacks, we identify three key, but interrelated,mechanisms that we believe are consistently important.

First, herbivores regulate the quantity of organic matter

that is returned to soil through inducing physiological

responses at the individual plant level, such as changes

in biomass production and resource allocation, fine root

dynamics, and root exudation (mechanism 1). Second,

herbivores alter the quality of resource inputs to the

decomposer subsystem either directly, through the re-

turn of feces and urine to soil, or indirectly by altering

concentrations of nutrients and secondary metabolites

in tissues, with implications for plant litter quality, de-

composition, nutrient supply, and ultimately ecosystem

function (mechanism 2). Third, at the plant community

scale, the effects of foliar herbivory on soil biota and

their functioning occur over much longer time scales

through altering the functional composition of vege-tation which may either enhance or reduce overall plant

litter quality and hence its decomposability (mecha-

nism 3). Herbivores are also likely to influence soil

processes through physical disturbance and alteration

of soil abiotic factors such as temperature and moisture

status. Here, we focus on the effects of herbivory on

producerdecomposer feedbacks that involve changes

in resource quality and quantity.

Mechanism 1: alterat ion of resource quantit y

There are two ways in which herbivory, both above-

ground and belowground, can alter the quantity of or-

ganic matter that is returned to soil. In the short term,

the quantity of resources supplied to soil can be altered

through effects of herbivory on plant C allocation and

root exudation patterns, whereas in the long term, the

amount of organic matter returned to soil is affected

by herbivore-induced shifts in net primary productivity

(NPP). Both these mechanisms are intimately linked

and collectively influence plant productivity at the

community level (Fig. 1).

In the short term, herbivory alters the quantity of

resources that are transferred to soil due to changes in

root exudation patterns. Plants allocate large propor-

tions of their assimilated C to root exudation (Bokhari

1977), which may stimulate the growth and activity of

heterotrophic microbes in the rhizosphere. Both foliar(e.g., Holland et al. 1996) and root (Yeates et al. 1998)

herbivory have been shown to increase root exudation

in grassland plants, which in turn stimulates microbial

biomass and activity in the rhizosphere (Denton et al.

1999, Hamilton and Frank 2001), and microbe-feeding

fauna (Mikola et al. 2001a). These facilitating effects

of herbivory on rhizosphere microbes, and presumably

higher level consumers in the soil food-web (Mikola

et al. 2001a), have been shown to positively feedback

on soil N availability, plant N acquisition, leaf N con-

tent, and photosynthesis of a grazing tolerant grass

(Poa pratensis), ultimately benefiting plant productiv-

ity in grassland of high soil fertility (Hamilton and

Frank 2001). Such benefits of these herbivoreplantmicrobial interactions might not only be restricted to

the individual plant that has been subjected to herbiv-

ory, but are also likely to benefit neighboring plants.

This is yet to be demonstrated with regard to foliar

herbivory. However, root herbivory of N-fixing white

clover (Trifolium repens) by clover cyst nematode

(Heterod erii trifoli) was shown to not only increase

root exudation and microbial activity in the rhizo-

sphere, but also increase the root growth and N content


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2260 RICHARD D. BARDGETT AND DAVID A. WARDLE Ecology, Vol. 84, No. 9

FIG. 1. Schematic of the effects of foliar and root herbivory on producerdecomposer feedbacks that result from changesin the quantity of resources returned to the soil. These mechanisms are most common in nutrient-rich grasslands, wheredominant plant species benefit from herbivory through positive feedbacks between herbivores, plants, and soil biota, andthrough preventing colonization by later successional plants which produce poorer litter quality. In unproductive and nutrient-poor ecosystems, compensatory plant growth responses to foliar herbivory will not occur, and declines in NPP caused byfoliar herbivory should cause reductions in soil organisms.

of a neighboring grass (Lolium perenne) (Bardgett et

al. 1999b).

There is evidence that these stimulatory effects of

herbivory on rhizosphere processes vary with the in-

tensity of foliar herbivory and with plant species iden-

tity (Guitian and Bardgett 2000, Mikola et al. 2001 a),

with the level of root infestation of the host plant (Den-

ton et al. 1999) and with the identity of the root-feeding

organism (Bardgett et al. 1999a). However, on the basisof the above findings, we might speculate that in grass-

lands of high soil fertility at least, such responses to

herbivory have the potential to stimulate rhizosphere

processes that ultimately feedback positively on plant

nutrition and photosynthesis, and hence plant produc-

tivity at the community level.

In the longer term, herbivory influences the quantity

of organic material that is returned to soil, and hence

to the decomposer food web, through shifts in NPP.

There are many instances where foliar herbivory by

large mammals has negatively affected aboveground

NPP (Milchunas and Lauenroth 1993). There is also

some experimental (e.g., McNaughton 1985) and the-

oretical (e.g., De Mazancourt et al. 1998) evidence thataboveground grazing enhances aboveground NPP at the

community level, especially in grasslands of high soil

fertility that are grazed at intermediate intensity. Direct

linkages between grazer-induced stimulation of above-

ground NPP and soil food webs have not been made.

However, in a field study of gradients of sheep (Ovis

aries) grazing intensity on British hill grasslands,

Bardgett et al. (2001) reported that soil microbial bio-

mass was maximal at intermediate levels of grazing

intensity, indicating that compensatory responses to in-

termediate levels of herbivory were probably related,

in part, to enhanced circulation of nutrients by soil

microbes (De Mazancourt et al. 1998) and are probably

intimately linked to the stimulation of rhizosphere pro-

cesses by herbivore-induced root exudation (Bardgett

et al. 1998b), as well as other direct plant physiological

responses to herbivory. Similarly, there is evidence that

moderate densities of invertebrate herbivory (i.e.,grasshoppers) can promote NPP through enhancing ni-

trogen cycling (Belovsky and Slade 2000). It is of note

that herbivory generally has an adverse effect on my-

corrhizal associations (Gehring and Whitham 1994),

suggesting that the optimization of decomposer organ-

isms at intermediate intensities of herbivory does not

usually apply to mutualists that are intimately associ-

ated with plant roots. Further, these patterns of opti-

mization of NPP by herbivores that are linked to the

stimulation of rhizosphere processes appear to be es-

pecially common in productive grassland sites, where

they typically reinforce conditions of high soil fertility.

They do not appear to be widespread in slower growing

forest ecosystems of relatively low soil fertility; Wardleet al. (2001) found no evidence of grazing optimization

of plant biomass at any of 30 fenced exclosure plots

in New Zealand forests.

There is mixed evidence about how foliar herbivory

affects root productivity. Pot experiments consistently

show that repeated defoliation reduces root biomass

(e.g., Guitian and Bardgett 2000, Mikola et al. 2001a),

and field studies have shown that moose and hare

browsing reduces fine root productivity in Alaskan Tai-


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ga forest (Ruess et al. 1998). However, exclusion stud-

ies on Serengeti grasslands show that mammalian graz-

ers do not necessarily inhibit root biomass and pro-

ductivity (McNaughton et al. 1998), and in a global

literature synthesis Milchunas and Lauenroth (1993)

reported both enhancements and reductions in root bio-

mass as a result of herbivore exclusion. There are nu-merous reports of root herbivores negatively affecting

NPP in a range of ecosystems (e.g., Brown and Gange

1990, Ingham and Detling 1990), and also incidences

where infestation of roots by insects has led to prolif-

eration in the growth of lateral roots (Brown and Gange

1990). However, examining the direct effects of root

herbivores on NPP in the field is extremely difficult

since plants are frequently damaged simultaneously by

foliar and root herbivores (Muller-Scharer and Brown

1995). Root feeding organisms may also indirectly af-

fect NPP by increasing the susceptibility of plants to

soil-borne pathogenic microorganisms (Van der Putten

et al. 2001), and mycorrhizal fungi might also be in-

volved in these multitrophic interactions, for exampleby competing with plant pathogenic fungi or through

plant defense (Van der Putten et al. 2001).

The knock-on effects of herbivore-induced changes

in NPP to the soil food web and nutrient cycling are

not at all clear. For example, increasing NPP has been

shown to have both positive and negative effects on

both microbial biomass and higher trophic levels of the

soil food web (reviewed in Wardle 2002). There are

two reasons for idiosyncratic responses of decomposers

to NPP. First, the relative importance of top-down and

bottom-up forces in regulating soil food web compo-

nents may be context dependent. Second, plants not

only provide carbon resources for microbes but also

compete with them for nutrients (Kaye and Hart 1997).Therefore, the direction of effects of herbivore-induced

changes in NPP on decomposer organisms and nutrient

cycling may be governed by which of two opposing

effects (stimulation of microbes by carbon addition,

inhibition of microbes by resource depletion) domi-

nates. However, despite this uncertainty, we propose

that positive effects of herbivory on soil biota and nu-

trient mineralization dominate in sites of high soil fer-

tility, especially in grasslands where carbon addition

to soil from plants typically stimulates soil biological

activity since it alleviates carbon limitation of mi-

crobes.

Mechanism 2: changes in resource qualityDung and urine return .Ungulate waste and its fa-

cilitative effect on soil biological processes is com-

monly promoted as one of the main driving mecha-

nisms for grazers stimulating N availability and plant

nutrient uptake at the plant community scale, especially

in grasslands of high fertility that carry large numbers

of gazing animals (e.g., McNaughton et al. 1997a, b,

Frank and Groffman 1998). Herbivorous mammals can

return large quantities of undigested and nonassimi-

lated nutrients to the soil as dung and urine. This ef-

fectively shortcuts the litter-decomposition pathway,

providing highly decomposable resources that are rich

in labile nutrients, and which can stimulate microbial

biomass and activity (Bardgett et al. 1998a), net C and

N mineralization (Molvar et al. 1993), and ultimately

plant nutrient acquisition and growth. Although the fa-cilitative effect on plantsoil interactions of this form

of nutrient redistribution is unquestionable, it has been

argued that it cannot explain the widely documented

positive effects of herbivores at large spatial scales

(Hamilton and Frank 2001). In agricultural and natural

ecosystems, waste patches typically only influence a

relatively small proportion of the surface area (Au-

gustine and Frank 2001) and, in some cases, the pos-

itive effects of animal wastes on soil processes are

insufficient to negate other, adverse effects of browsing

(Pastor et al. 1988). Remarkably little is known about

the effects of waste from invertebrate herbivores on

soil processes, although in microcosms frass from lar-

vae of the gypsy moth (Lymant ria dispar), which hadfed on foliage of Quercus velutina, has been shown to

increases in microbial growth and N mineralization in

soil (Lovett and Ruesink 1995). As with larger herbi-

vores, the effects of invertebrate waste products on soil

processes are probably highly localized, and may not

be able to explain herbivore effects on soil processes

at large spatial scales. Further, since ecosystems have

a high degree of spatial structure with local variability

in soil resources (Schlesinger et al. 1996), these lo-

calized effects of herbivores on soil nutrient supply will

potentially exert strong effects on this variability, often

increasing the heterogeneity of resources entering the

soil (Augustine and Frank 2001). Such heterogeneity

within ecosystems may create hotspots of produc-tivity, which presumably will alter the magnitude of

herbivore effects on soil biota and soil processes at the

local scale.

Leaf and root litter quality .Foliar herbivory in

grasslands of high soil fertility often enhances leaf nu-

trient concentration (e.g., Holland and Detling 1990,

Hamilton and Frank 2001) either directly through re-

allocation of nutrients within individual plants, or in-

directly by stimulating soil mineralization processes,

as discussed above. Likewise, in forest ecosystems,

there are incidences where browsing by mammals has

been reported to enhance nutrient concentrations and

reduce levels of carbon-based secondary metabolites,

such as phenolics, in foliage (Bryant and Reichart1992). This has been shown to improve the quality of

leaf litter being returned to soil, thereby enhancing de-

composition and mineralization processes in forest eco-

systems (Keilland et al. 1997). Stimulation of soil biota

and soil processes by foliar herbivory may also be due,

in part, to roots of grazed plants producing litter of a

higher quality. Seastedt et al. (1988) showed that trim-

ming of shoots of the grass Andropogon gerardii in-

creased the N concentration of roots, and proposed that


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this would stimulate soil organisms through improved

resource quality. Likewise, root herbivory has been

shown alter the root N content of plants attacked by

nematodes (Bardgett et al. 1999a, b). Such herbivore-

induced increases in foliage and root nutrient concen-

tration will invariably feedback positively on soil biota

and soil mineralization processes.Herbivores can also induce the production of sec-

ondary plant compounds in foliage and roots, which

negatively impacts on soil biota due to reduced litter

quality. For example, severe defoliation of trees, such

as that caused by periodic invertebrate attack, often

results in reduced concentrations of N and increased

concentrations of certain secondary metabolites (e.g.,

phenolics) in subsequently produced foliage. It is un-

clear whether this response is induced for plant de-

fense against browsing (Rhoades 1985) or whether phe-

nolic production is a physiological response of trees

recovering from the nutritional deficiency associated

with defoliation (Bryant et al. 1993). Whatever the

mechanism responsible, the net result is likely to bethe production of leaf litter with characteristics that are

less favorable for decomposer organisms. Direct evi-

dence of this is scarce, but Findlay et al. (1996) showed

that cellular damage caused by spider mites to seedlings

of Populus deltoides increased the concentration of

polyphenols in foliage, resulting in a 50% reduction in

the decomposition rate of subsequently produced leaf

litter. The importance of these events in nature is not

known, but presumably they would negatively influ-

ence soil mineralization processes and plant produc-

tivity at the individual plant and plant community scale.

Numerous other antiherbivore defenses are produced

in shoots of herbaceous plants in response to herbivore

attack (Agrawal 1998) and several defense compoundsinvolved in aboveground defense are produced in roots,

and then transported aboveground (Van der Putten et

al. 2001). Almost nothing is known about how these

induced antiherbivore defense compounds persist in lit-

ter produced by herbivore-attacked plants, or how they

may affect components of the soil biota and soil min-

eralization processes. However, their impact on pro-

ducerdecomposer feedbacks is complex and therefore

difficult to predict because their induction following

herbivore attack might also affect plant-pathogen in-

teractions (Paul et al. 2000) or act as a cue for para-

sitoids and predators of the herbivore, thereby reducing

herbivore attack. This latter mechanism has recently

been demonstrated for both foliar herbivore (Kesslerand Baldwin 2001) and root herbivore (Van Tol et al.

2001) attack. These multitrophic and nutritional inter-

actions will influence the net effect of herbivory on

plant growth and make the outcome of producerde-

composer feedbacks difficult to predict.

Mechan ism 3: functional composition of vegetation

Over long time scales, herbivory often leads to sig-

nificant changes in the functional composition of the

plant community, which in turn alters not just the quan-

tity, but also the quality of litter inputs to soil, and

hence affects soil biota and soil nutrient cycling.

Across plant species, palatability of foliage and de-

composability of plant litter are governed by similar

suites of ecophysiological traits, and for this reason

palatable plant species generally produce litter that isof a higher quality for decomposers than do unpalatable

species (Grime et al. 1996). The influence of herbivores

on plant species replacement and vegetation succes-

sion, and associated changes in the functional com-

position of vegetation, can therefore be important in

driving the belowground subsystem. Several examples

in the literature exist both of retardation and acceler-

ation of plant succession by herbivores (reviewed by

Davidson 1993), and these effects are likely to impact

upon the decomposer subsystem (Fig. 2). Retardation

of succession occurs when dominant plant species ben-

efit through herbivory, for example through compen-

satory growth and positive feedbacks between plants

and herbivores (Augustine and McNaughton 1998).This mechanism is most common in grasslands of high

soil fertility, and here herbivory has positive effects on

the decomposer subsystem through preventing colo-

nization by later successional plants which produce

poorer litter quality, as well as through returning carbon

and nutrients to the soil in labile forms as dung and

urine. Since herbivore diversity is positively related to

soil nutrient availability on global scales (Olff et al.

2002) it is likely that existence of these positive feed-

backs that involve soil biota are instrumental in sus-

taining global hot spots of herbivore diversity.

Acceleration of succession tends to occur in low-

productivity ecosystems of low soil fertility and results

from browsed plant species being disadvantaged by

herbivory, and results in replacement of palatable plant

species by species which are better defended against

herbivory but produce litter of poorer quality. For ex-

ample, Pastor et al. (1988) found that browsing by

moose on deciduous tree species with nutrient-rich fo-

liage increased the dominance of a Picea spp., which

is of low palatability and produces litter of poorer qual-

ity. This shift in vegetation composition resulted in

reduced soil microbial biomass and slower rates of lit-

ter decomposition and soil N mineralization, thereby

reducing soil N availability and plant productivity.

Similarly, insect and mammalian herbivory in N-lim-

ited Oak savanna was shown by Ritchie et al. (1998)to greatly decrease the abundance of plant species with

N-rich tissue (especially the legume Lathyrus venosus),

thereby reducing the positive contribution of these

plants on N cycling in these ecosystems.

While several studies have shown effects of above-

ground herbivory on plant succession, information on

the effects of root herbivores on vegetation change and

resulting producerdecomposer feedbacks is scarce.

What evidence is available suggests that root herbivory


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FIG . 2. Mechanistic basis of how herbivores affect the decomposer subsystem at a plant community level, through alteringsuccessional trajectories.

can accelerate plant succession, and is therefore likelyto also indirectly affect the soil biota and soil processes

through changes in the quality of resource inputs to

soil. For example, root herbivory by plant-feeding

nematodes was found to induce the degeneration of

Marram grass (Ammophila arenaria), leading to its re-

placement by the grass Festuca rubra (Van der Putten

and Peters 1997). Likewise, in grassland, root-feeding

nematodes might have contributed to small-scale shifts

in vegetation composition of grassland (Olff et al.

2000), and to accelerated succession of grass species

in agricultural grassland, especially when N becomes

limiting after fertilization is stopped and plants become

more susceptible to nematode attack (Verschoor 2001).

Root herbivores can also alter secondary succession ingrassland by selectively feeding on N-rich seedlings,

thereby increasing seedling mortality (Brown and Gan-

ge 1992). All these herbivore-induced changes in plant

community composition will alter the quality of litter

entering the soil, thereby influencing soil biota and soil

processes. However, the direction and nature of these

potential producerdecomposer feedbacks, and their

interrelationship with other indirect effects of root her-

bivory (e.g., increased susceptibility to pathogen at-

tack), remains unknown and is extremely difficult topredict.

An additional role for root herbivores in plant suc-

cession and producerdecomposer feedbacks concerns

their effects on N transfers from early successional N

fixing plants. It has been reported that nematode feed-

ing on a legume increased the transfer of N from this

plant to a neighboring grass species, and that the trans-

fer was facilitated by increased microbial activity in

the rhizosphere of the infested plant (Bardgett et al.

1999b). If these responses are common in legume-her-

bivore associations, then it is likely that they would

contribute to facilitative effects of N-fixers in plant

succession. For example, root-herbivore induced en-

hancements in nutrient flux in the rhizosphere of nat-urally occurring N2-fixers, such as alder (Alnus spe-

cies), may benefit other successional plant species, thus

contributing to species replacement (Fig. 3). These

ideas remain untested, but the widespread occurrence

of N-fixers in primary succession and their strong as-

sociation with host-specific root herbivores suggests

that such interactions might have an important role in

determining vegetation change and soil nutrient cycling

in natural ecosystems.


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FIG. 3. Proposed facilitative role for root herbivores in plant succession through their positive effect on N transfers fromearly-successional N-fixing plants to late-successional plant species, contributing to plant species replacement. These facil-itative effects are likely to occur in association with other inhibitory effects of root herbivores and pathogen attack on theearly-successional N fixer, thereby contributing to the displacement of early-successional species.

THE SIGNIFICANCE OF

MULTIPLE-HERBIVORE-SPECIES COMMUNITIES

The vast majority of studies on herbivore impacts in

ecosystems have focused on a single species of her-

bivore. However, in real ecosystems, several species of

herbivore usually coexist, and may indirectly interact

with one another (Masters and Brown 1997, Van derPutten et al. 2001). It is therefore plausible that mul-

tiple-species herbivore communities may exert very

different effects on community- or ecosystem-level

properties (including those relevant to the decomposer

subsystem) to what would be observed for single her-

bivore species systems. The ecological consequences

of increasing herbivore diversity (at either the species

or functional group level) may be expected to operate

through the same types of mechanisms that have been

proposed for ecosystem effects of plant diversity, in

which greater resource partitioning among species and

greater difference between species in key functional

attributes maximizes the net effect of diversity (Nijs

and Roy 2000, Daz and Cadibo 2001).At the within-plant level, resource partitioning, and

therefore resource-use complementarity among herbi-

vore species, is maximized when different herbivore

species belong to different functional groups or guilds

(cf. Root 1973) and utilize different tissues of the same

plant. Similarly, at the level of the plant community,

resource partitioning among herbivore species is most

likely to occur when the herbivore community is dom-

inated by specialists which selectively feed on different

plant species, and least likely when the community is

dominated by generalists that are in competition for

the same food resource. Greater resource partitioning

through increased herbivore diversity would in turn be

expected to lead to greater net resource utilization

(through greater net consumption of plant material) by

the herbivore community.It is well recognized that the effects of increased

plant species diversity on production-driven processes,

through greater total resource utilization, can only op-

erate in a positive direction (Fig. 4a). In contrast, in

the case of herbivores, greater net resource utilization

through increased diversity can theoretically result in

a range of possible effects on ecosystem processes (Fig.

4b). This is because, as explained in the earlier dis-

cussion, there are a variety of mechanisms through

which increasing intensities of herbivory can affect the

quantity and quality of resources entering the decom-

poser subsystem, and both positive and negative effects

may arise depending upon the relative importance of

different mechanisms. Further, it is possible that, withina system, increasing net consumption of plant material

(through increasing herbivore density) may not only

lead to just montonically increasing or decreasing eco-

system process rates, but also unimodal responses, be-

cause plant-driven processes can be optimized by in-

termediate levels of herbivory.

Although Fig. 4 provides a theoretical framework

about how herbivore diversity may influence ecosystem

processes, there are few studies that have provided rel-


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FIG . 4. (a) The types of responses that may be expected for plant productivity and related ecosystem functions to increasingplant diversity, and (b) the response of ecosystem functions that can theoretically occur as a result of increasing herbivore

diversity through resource use complementarity. Both positive and negative responses of belowground processes are possiblebecause increasing net herbivory (resulting from greater resource use complementarity) can have either positive or negativeeffects on decomposer organisms depending upon which mechanisms are dominating. Further, unimodal responses cantheoretically occur if plant productivity and nutrient cycling rates are optimized by intermediate levels of herbivory.

evant data. At the within-plant level, it is recognized

that resource partitioning among herbivore species may

occur, for example, where different species utilize dif-

ferent tissues produced by the same plant (Masters and

Brown 1992) or utilize tissues of that plant at different

times of the year (see Masters et al. 1993). Further,

Masters and Brown (1992) and Muller-Scharer and

Brown (1995) both considered the net impact of above-

ground and belowground herbivores, both singly and

in combination, on plant production; neither studyfound consistent interactive effects of both herbivore

groups together as opposed to each one operating sin-

gly. However, the issue of how resource partitioning

among different herbivore species or functional groups

consuming the same plant influences the quality and

quantity of resources produced by the plant, and the

consequences of this for the decomposer subsystem,

remains essentially unexplored.

At the level of the plant community, some degree of

specialization among herbivore species (and therefore

resource partitioning) can be inferred by the frequently

observed pattern of herbivore species diversity being

correlated with plant species diversity (Southwood et

al. 1979). There is a dearth of studies addressing thebelowground functional significance of herbivore di-

versity, although relevant data is presented by the ex-

perimental work of Mikola et al. (2001b). Here, syn-

thetic plant communities of three grassland plant spe-

cies were established, and treatments consisted of de-

foliation of the three species in all one-, two-, and

three-way combinations. Indirect effects of defoliation

were found to differ across treatments for some com-

ponents of the soil food web, soil respiration and soil

nitrate levels, and these effects were determined by

which combinations of species were defoliated rather

than how many species were defoliated. Further, War-

dle et al. (2000) found for synthesized plantherbivore

grassland communities that the effects of two inver-

tebrate herbivore species in combination on various

above- and belowground properties and processes gen-

erally did not differ from that of each of the two her-

bivore species considered singly. This points to the two

species being able to substitute for the effects of oneanother. Some evidence for the possible ecosystem-

level importance of resource use complementarity vs.

competition among herbivore species emerges from the

browsing mammal literature. For example, Bowers

(1993) used fenced exclosure plots in which four dif-

ferent types of exclosures were used to selectively ex-

clude different components of the mammalian herbi-

vore community based on animal body size, and found

that different subsets of the mammalian herbivore biota

differed in their overall effects on the plant community.

However, comprehensive experimental tests of the eco-

system impacts of terrestrial herbivore diversity, at ei-

ther the functional group level or species level (e.g.,

along the lines of those recently performed for estua-rine herbivore systems by Duffy et al. [2001]), remain

to be conducted.

CONCLUSIONS

In this paper, we have identified and proposed three

key mechanisms by which herbivores can indirectly

affect decomposer organisms and soil processes

through altering the quantity and quality of resources

that enter the soil. These mechanisms appear to be


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broadly similar in nature for both foliar and root her-

bivory, and mechanisms resulting from both operate at

a range of spatial and temporal scales. These can op-

erate either in the short term, through involving phys-

iological responses of individual plants to herbivore

attack, or in the long term, involving alteration of plant

productivity and community structure and subsequentchanges in the quantity and quality of litter inputs to

soil. Due to the variety of possible mechanisms, the

effects of foliar and root herbivores on soil biota and

ecosystem function are idiosyncratic and hence diffi-

cult to predict, with positive, negative, or neutral ef-

fects of herbivory being possible depending upon the

balance of these different mechanisms. The variety of

mechanisms is consistent with the idiosyncratic and

heterogeneous nature of herbivore impacts that are

commonly observed in the field.

What is clear is that the magnitude of herbivore ef-

fects on soil biota and soil processes, and the conse-

quence of this for producerdecomposer feedbacks,

differs greatly across ecosystems, and this appears todepend largely on soil fertility, a determinant of her-

bivore diversity (Olff et al. 2002), and on the proportion

of NPP that is consumed by herbivores. The proportion

of NPP that is consumed by herbivores varies consid-

erably across ecosystems (McNaughton et al. 1989),

and in more productive ecosystems, which are domi-

nated by palatable, nutrient-rich plants and support a

greater diversity and level of herbivory, positive effects

on soil biota and soil processes appear to dominate.

Here, a key mechanism for these positive effects of

herbivory is that nutrients are returned to the soil in

labile forms (e.g., dung and urine, and high quality

litter) leading to positive effects on soil biota and min-

eralization processes, and hence plant productivity(mechanism 2). Additionally, plant physiological re-

sponses to herbivory, such as enhanced root exudation,

also stimulate soil biota and nutrient mineralization

processes in productive ecosystems (mechanism 1),

leading to enhanced nutrient supply to plants. These

mechanisms, together, reinforce soil fertility and ulti-

mately benefit plant productivity at the ecosystem

scale. In contrast, in unproductive ecosystems of low

soil fertility, with low herbivore consumption rates,

negative effects on soil biota and soil processes appear

to dominate. Here, selective grazing leads to changes

in the functional composition of vegetation (mecha-

nism 3), and especially the dominance of defended

plant species that produce litter that is of poor nutri-tional quality to decomposers. The net effect of this is

low levels of soil biotic activity, nutrient mineraliza-

tion, and supply rates of nutrients from soil, and hence

a reduction in plant productivity at the ecosystem scale.

While positive effects on soil biota may occur in these

unproductive ecosystems, for example due to fecal re-

turn, these effects are likely to be highly localized and

hence of relatively little importance to plant produc-

tivity at the ecosystem scale.

We highlight some directions for future research on

the effects on herbivory and producerdecomposer

feedbacks. First, and perhaps most importantly, there

is a need for comprehensive field studies that compare

the nature, and determine the underlying mechanisms,

of herbivore impacts on aboveground and belowground

processes in ecosystems of varying productivity andsoil fertility. Second, more studies are required to ex-

plore the various ways that root herbivores impact on

soil biota and soil processes. In particular, there is a

need for experimental testing of their roles in relation

to how root herbivores with differing feeding strategies

and degrees of host specificity indirectly influence the

soil subsystem, and how their impacts are modified by

complex multi-trophic interactions (for example be-

tween plants, root herbivores, and pathogens). A re-

lated question that requires testing is how predation of

both foliar and root herbivores influences soil biota and

soil processes by causing trophic cascades which could

affect the quantity and quality of resources produced

by plants. Third, a key challenge is to further our un-derstanding of how plants and soil biota respond to

simultaneous attack from root and foliar herbivores,

and to simultaneous attack from the diversity of her-

bivores that can exist both above and belowground. To

this end, we have presented various predictions that

require experimental investigation on the range of re-

sponses of soil biota and soil processes that can the-

oretically occur as a result of increasing herbivore di-

versity through resource use complementarity. Finally,

virtually nothing is known about how induced anti-

herbivore defense compounds may directly affect com-

ponents of the soil biota and soil mineralization pro-

cesses, or how they might indirectly influence the soil

subsystem through altering multitrophic interactionsbetween herbivores, parasitoides and predators; un-

derstanding of these multitrophic interactions is clearly

a key research challenge.

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Ecolog y, 84(9), 2003, pp. 22692280 2003 by the Ecological Society of America

PLANT DEFENSE BELOWGROUND AND SPATIOTEMPORAL PROCESSESIN NATURAL VEGETATION

WIM H. VAN DER PUTTEN1

Netherlands Institute of Ecology NIOO-KNAW, Multitrophic Interactions Department, P.O. Box 40,6666 ZG Heteren, The Netherlands

Abstract. Root herbivores and pathogens play an important role in driving plant abun-dance, species diversity, and succession in natural vegetation. Subterranean plant feedersand pathogenic microorganisms interfere with basic functions of plant roots, such as re-source uptake, storage of reserves, and anchoring of plants in the soil, but concepts andtheories on control of herbivores and pathogens, such as the Green World Hypothesis, havebeen developed and applied almost exclusively for the aboveground subsystem. Root her-bivores and pathogens affect spatial and temporal patterns in natural plant communities,and whether these patterns are cyclic or irreversible depends on characteristics of the rootfeeders, interactions with other soil or aboveground organisms, and the rate of changes inthe abiotic environment. Established plants can tolerate root herbivores and pathogens atdensities that are lethal to their offspring. Dispersal by seeds or rhizomes allows new cohortsto become established before root herbivores or root pathogens colonize and develop, but

it provides only temporal release of plants from their natural enemies. Permanent releasefrom root herbivores and pathogens contributes to plant invasiveness. I propose to expandthe concept of plantsoil feedback by including plant defense belowground. Many plantsecondary compounds are synthesized in the roots, and these chemicals could affect rootherbivores, root pathogens, and their natural enemies. Plants may exert direct and indirectdefense, resistance, tolerance, or dispersal to move away from the herbivores and pathogensbelowground, and I propose that acknowledging trade-offs and life history strategies willenhance our capacity to predict spatiotemporal patterns in natural vegetation. Further studiesin this area will enhance our understanding of plant abundance, succession, and invasionsin natural communities, as well as the evolution of plant dispersal and other defensivestrategies against root herbivores and pathogens in natural communities.

Key words: direct and indirect defense; dispersal; diversity; enemy release; invasiveness; mul-titrophic; nematode; plant community; resistance; root pathogen; subterranean herbivore; succession.

INTRODUCTIONMany soil organisms have the potential to influence

the composition of plant communities in space and

time, either through changing the availability of re-

sources, or by direct feeding on plant roots (Wardle

2002). Plants affect soil organisms and soil organisms

reciprocally affect plants, leading to a feedback that

drives changes in plant communities over space and

time (Bever et al. 1997). The feedback between plants

and soil organisms can be positive, neutral, or negative

for the plants involved, for their offspring, and for other

plant species in the community (Reynolds et al. 2003).

In order to enhance our understanding of plantsoil

feedback in relation to plant life histories and plant

community processes, interactions between plants andthe various functional groups of organisms inhabiting

the root zone need to be explored in more detail.

I will focus mainly on interactions between plant

roots, invertebrate herbivores, microbial pathogens,

Manuscript received 8 May 2002. revised 4 October 2002.accepted 12 October 2002; final version received 11 November2002. Corresponding Editor: A. A. Agrawal. For reprints of thisSpecial Feature, see footnote 1, p. 2256.

1 E-mail: [email protected]

mutualistic symbionts, and natural enemies of the her-bivores and pathogens. These interactions below

ground may contribute to the relative abundance of

plant species (Gange et al. 1993, Klironomos 2002),

plant species diversity (Bever 1994, Holah and Alex-

ander 1999, Packer and Clay 2000, De Deyn et al.

2003), primary succession (Van der Putten et al. 1993),

secondary succession (Brown and Gange 1992, Holah

and Alexander 1999, Callaway et al. 2000, Verschoor

et al. 2001, De Deyn et al. 2003), and possibly also to

plant invasiveness (Klironomos 2002). I propose that

these plant community processes are strongly affected

by plant defense belowground.

In general, plant defensive strategies may include

tolerance, resistance, direct and indirect defense, ormoving away from their above- and belowground her-

bivores or pathogens (Burdon 1987, Karban and Bald-

win 1997). Plant defense theory that includes the nat-

ural enemies of herbivores (Price et al. 1980), has been

almost solely developed and tested for aboveground

interactions (Van der Putten et al. 2001). In soil, most

studies have focused on plantherbivore or plantpath-

ogen interactions, and in spite of a vast amount of

biocontrol research on belowground invertebrate her-


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2270 WIM H. VAN DER PUTTEN Ecology, Vol. 84, No. 9

bivores and pathogens in crop systems, very little is

known on the role of natural enemies of root herbivores

and pathogens in the feedback between plant and soil

communities. Since the number of examples of root

herbivores and pathogens in natural plant communities

is steadily increasing, we now can start examining plant

defense from a belowground perspective in order tofurther understand spatiotemporal processes in natural

vegetation and plant life history evolution.

Here, I focus on direct and indirect interactions be-

tween living plant roots and soil organisms, explore

examples of plantherbivore/pathogen interactions in

natural ecosystems, and discuss current ideas investi-

gating how plants may avoid, tolerate or resist, or de-

fend themselves against root herbivores and root path-

ogens.

ROOT HERBIVORES, ROOT PATHOGENS,

AND HOST SPECIFICITY

Most root herbivores are invertebrates (insects, mi-

cro-arthropods, and nematodes), though vertebrates,mainly small mammals, also feed on plant roots (Mor-

timer et al. 1999). As far as microorganisms are con-

cerned, the majority of the examples of soil pathogens

in natural vegetation concern fungal diseases (Jarosz

and Davelos 1995). Detailed reviews have highlighted

the effects of root-feeding insects (Andersen 1987,

Brown and Gange 1990), root-feeding nematodes

(Stanton 1988, Mortimer et al. 1999), and root path-

ogens (Jarosz and Davelos 1995), and how these affect

the productivity and composition of natural plant com-

munities. I will focus on host specificity and, briefly,

on dispersal of root herbivores and root pathogens,

since these are important features for plant defense

belowground.Host specificity varies widely between belowground

insect herbivores (Mortimer et al. 1999). The larval

stages of root herbivorous insects, as well as the other

root herbivores and pathogens have limited active dis-

persal capacity, usually ranging from a few centimeters

up to a meter per year (Mortimer et al. 1999, Gormsen

2001). However, active dispersal, such as of the above-

ground stages of some root-feeding insect larvae, may

facilitate host location (Nordenhem and Eidmann

1991). Microarthropods, nematodes and soil microor-

ganisms are dispersed passively by wind (Orr and New-

ton 1971, Griffin et al. 2001), which does not favor the

development of host specificity. Specific root feeding

nematodes are mainly known in agricultural ecosys-tems, where crop rotation leads to the predictable pres-

ence of host plants. Specificity also occurs in temperate

coastal foredunes, where natural plant species typically

occur in monospecific stands. Some nematode species,

such as Meloidogyne duytsi on Elymus farctus (sand

twitch) and M. maritima on Ammophila arenaria (mar-

ram grass) occur on a single host-plant species (Van

der Putten and Van der Stoel 1998). Probably, the pre-

dictability and reliability of the presence of host plant

roots favors selection for specialization in root-feeding

nematodes in sand dunes.

Microorganisms have poorer active dispersal abili-

ties, for example, through hyphal growth, than most

invertebrates (De Boer et al. 1998b). Specialists might

also develop in the case of facultative saprotrophic

growth of soil pathogens, such as oomycete fungi,which survive the absence of their host plants by feed-

ing on dead organic matter (Jarosz and Davelos 1995).

An example of this group of facultative saprotrophs is

Pythium sp., which kills seedlings of Prunus serotina

(black cherry) in North American forests (Packer and

Clay 2000). However, facultative saprotrophic species

are inferior competitors for dead organic matter and

will, sooner or later, be outcompeted by obligatory sap-

rophytes unless host plants become re-established. Oth-

er strategies that might favor the development of host

specificity of nematodes and soil microorganisms are

the formation of survival structures (cysts, dauer lar-

vae, spores) which enables these organisms to survive

periodic absence of the hosts.

PLANT DEFENSE STRATEGIES AGAINST ROOT

HERBIVORES AND ROOT PATHOGENS

After publication of the Green World Hypothesis

(Hairston et al. 1960), a major debate arose as to wheth-

er herbivores were controlled more effectively by re-

sources or predators. Alternatively, it was argued that

there is an arms race between plants and herbivores

leading to the evolution of plant chemical defense (Ehr-

lich and Raven 1964). Nowadays, it is generally ac-

cepted that evolutionary processes and resulting ad-

aptation from interactions between plants and herbi-

vores cannot be fully understood without including the

antagonists of the herbivores in a multitrophic frame-work (Price et al. 1980), although such approach has

rarely been applied to belowground interactions. In-

terestingly, studies on aboveground plant pathogens

have typically focused on disease resistance and co-

evolution of plants and pathogens (Burdon 1987),

whereas studies examining control of natural plant

pathogens by their natural enemies are rare (Yang et

al. 1993). Studies on aboveground plantherbivore and

plantpathogen interactions have pointed to a number

of defense responses by plants and possible trade-offs.

I will apply and develop these ideas for belowground

defense in relation to plant life history strategies and

plant community processes.

Avoidance and escape

Avoidance and escape have been studied in relation

to both aboveground and belowground herbivores and

pathogens. Plants may avoid their herbivores or path-

ogens through processes known as phenological es-

cape, whereby they flower early (or late) in the growth

season, or exhibit spatiotemporal unpredictability (Van

der Meijden et al. 1988). Phenological escape also in-

cludes the postponement of, for example, flowering un-


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til a reliable cue has indicated low risk of future attack

(Agrawal 2000).

The capacity of plants to produce roots in late au-

tumn and early spring is an example of avoiding root

herbivores and soil pathogens, as growth continues

when the herbivores and pathogens may be relatively

inactive. Seed dispersal (Packer and Clay 2000), clonalgrowth (De Rooij-Van der Goes et al. 1995), and dor-

mancy enable plants to avoid or escape from root her-

bivores and pathogens. Similar to some plants that re-

spond positively to aboveground herbivores (Agrawal

2000), exposure to mycorrhizal fungi increases the in-

tensity of rhizome branching (Streitwolf-Engel et al.

1997), whereas pathogens stimulate unidirectional rhi-

zome growth (DHertefeldt and Van der Putten 1998).

Tolerance and resistance

The capacity of plants to regrow and reproduce fol-

lowing herbivory is called tolerance (Strauss and Agra-

wal 1999). Similarly, tolerance for diseases is ex-

pressed as the performance of individuals in the pres-ence compared to their performance in the absence of

pathogens (Burdon 1987). Herbivory may even lead to

overcompensation, which can increase fitness (Agrawal

2000). Overcompensation occurs especially at low den-

sities of the grazers (Crutchfield and Potter 1995), and

it also expressed by fungal hyphae in soil when exposed

to low densities of enchytraeids (Hedlund and Au-

gustsson 1995). Plant roots may also exert such a com-

pensatory response at low nematode densities.

Whereas tolerant plants allow herbivores and path-

ogens to develop and reproduce, resistant plants reduce

the performance of their enemies (Karban and Baldwin

1997). In agricultural systems, tolerance and resistance

have been studied for above- and belowground herbi-vores, as well as for shoot and root pathogens. For

natural systems, on the other hand, tolerance and re-

sistance have been mainly studied in relation to above-

ground herbivores and pathogens.

Tolerance and other defense mechanisms, such as

resistance, are considered alternative plant traits in

plant-herbivore interactions (Van der Meijden et al.

1988). High growth rates enhance the competitive abil-

ity of plants, but it may come at the expense of their

capacity to defend against herbivores (Herms and Matt-

son 1992). Tolerance might be favored when resistance

is not possible, or very costly (Agrawal 2000). Em-

pirical support to trade-offs between tolerance and de-

fense are idiosyncratic (Strauss and Agrawal 1999).Probably, experimental conditions are crucial for the

results obtained. In controlled conditions, a large frac-

tion of plant root systems can be removed without neg-

atively affecting plant production (Van der Veen 2000),

however, selective root feeding reduces production of

susceptible plants when competing with resistant spe-

cies (Van der Putten and Peters 1997).

Tolerance may evolve when, for example, plant at-

tack by multispecies communities of pathogens is in-

evitable. In this case, avirulence is less likely to de-

velop (Roy et al. 2000). Soil communities will usually

consist of multispecies communities, so that root path-

ogens can be expected to be moderately aggressive.

Some soil pathogens, however, are so aggressive that

they kill all establishing plants (Packer and Clay 2000).

There is no evolutionary penalty for such aggressive-ness, as the pathogens concerned are facultative sap-

rophytes, which enables feeding on organic matter and

dead plant parts (Jarosz and Davelos 1995). Tolerance,

therefore, might not be the ideal solution for plant de-

fense against facultatively saprotrophic root pathogens.

In model calculations, resistant species should often

coexist with other, less resistant competing species

(Chase et al. 2000). In the same models, tolerant species

could not coexist with other, less tolerant competitors.

According to these models, species-rich plant com-

munities are expected to be mixtures of plant species

that resist root herbivores and soil pathogens, and oth-

ers that are tolerant.

Direct defense

A number of secondary plant compounds are pro-

duced, or presynthesized, in roots and then transported

to other plant organs (Karban and Baldwin 1997). Ex-

amples are pyrrolizidine alkaloids of Senecio jacobea

(Vrieling and Van Wijk 1994). Host plant secondary

defense chemicals are able to affect the performance

of root-feeding insect larvae (Brust and Barbercheck

1992), as well as entomopathogenic nematodes that

feed on the insect larvae (Jaworska and Ropek 1994).

These effects might be positive or negative for second-

and third-trophic-level organisms, although studies on

effects of plant chemicals on natural enemies of the

belowground herbivores or pathogens are scarce andcausal effects are difficult to establish. Root chemicals

that affect root-sucking insects have been rarely re-

ported (Brown and Gange 1990). There is also little

information on direct effects of secondary plant chem-

icals on root-feeding nematodes.

There is very little information on the effects of plant

defensive compounds on root pathogens and their nat-

ural enemies. Fungal pathogens (Fusarium oxysporum)

collected from roots of Senecio jacobea (common rag-

wort) performed better on alkaloids from S. jacobea

than the same fungi which had been collected from

other plant species (Hol and Van Veen 2002). Possibly,

plant defense compounds select for certain rhizosphere

microorganisms, but the feedback effects to plant per-formance and consequences for plant community pro-

cesses have not yet been studied.

Indirect defense

A main question in relation to indirect defense is

whether plants may be actively involved in recruiting

the enemies of their enemies (Dicke and Vet 1999,

Thaler et al. 1999). Entomopathogenic nematodes can

be recruited by plant roots through unknown attractants


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that are released from the roots upon larval feeding

(Van Tol et al. 2001, Boff et al. 2002). However, there

are comparatively few other examples of active re-

cruitment of third-level soil organisms by plants. Be-

lowground signals will operate over much smaller

scales than is the case above ground, because poor

diffusion and transport rates of volatiles and solublechemicals inhibit the spread of these compounds.

Antagonists of root herbivores and pathogens are

well known in agriculture, but the development of ef-

fective population densities lags behind their hosts,

sometimes requiring years of monocropping before ef-

fective control levels have been achieved (Weller et al.

1995, Kerry and Crump 1998). In natural systems,

therefore, short-lived plants might experience little

benefit from such antagonists, because they will be

replaced by more resistant plant species before antag-

onists have even developed an effective population

density. Nevertheless, antagonists of soil pathogens

have been observed in natural soils (Holah and Alex-

ander 1999), but these also directly affect root patho-gens without any involvement of plant roots (De Boer

et al. 1998a, b).

Arbuscular mycorrhizal fungi have been reported to

act as antagonists of root pathogens (Carey et al. 1992,

Newsham et al. 1994, 1995), plant-feeding nematodes

(Little and Maun 1996, Roncadori 1997), and root-

feeding insects (Gange 2000). Similarly, endophytic

fungi are able to reduce plant sensitivity to herbivorous

nematodes (Clay 1991).

Pathogenic rhizobacteria can induced systemic ac-

quired resistance (SAR) and nonpathogenic rhizobac-

teria can induce systemic resistance (ISR) against plant

pathogens (Van Loon et al. 1998). The rhizosphere bac-

teria that induce resistance, for example fluorescentPseudomonas spp., need to be present in sufficiently

high densities in order to be effective (Van Loon et al.

1998). Most of this work has been done on crop plants

and Arabidopsis thaliana. Theoretically, indirect de-

fenses against root herbivores and pathogens might be

operating in many natural systems, but their importance

for spatiotemporal processes in natural plant commu-

nities has received little attention.

PLANT COMMUNITY PROCESSES IN RELATION TO

BELOWGROUND DEFENSE STRATEGIES

The question of what drives changes in the com-

position of natural plant communities has been a re-

current theme in ecology, but it has only recently beenacknowledged that root herbivores and root pathogens

can influence these processes. Root herbivores and

pathogens affect primary (Van der Putten et al. 1993)

and secondary succession (Brown and Gange 1992,

Verschoor et al. 2001, De Deyn et al. 2003), as well

as plant dispersal (Packer and Clay 2000), plant species

diversity (Bever 1994, De Deyn et al. 2003), and abun-

dance or invasiveness of alien plant species (Kliron-

omos 2002). I propose that there is a relationship be-

tween plant defense belowground and the plant com-

munity processes that are observed in the field.

Primary succession

In coastal dunes of Europe, the nitrogen-fixing shrub

Hippophae rhamnoides (sea buckthorn) is highly vig-

orous in outer dunes, whereas, along a transect fromforedunes towards the inland, the shrubs die back and

gradually disappear from the vegetation. Initially, it

was supposed that root-feeding nematodes, such as Ty-

lenchorhynchus microphasmis, were causing the die-

back patterns (Oremus and Otten 1981). Subsequent

studies, however, have shown that nematodes alone

cannot cause the observed growth reduction (Maas et

al. 1983), and that plant pathogenic fungi may be in-

volved as well (Zoon et al. 1993). The precise mode

of interaction still needs to be resolved. Similarly, both

root-feeding nematodes and root pathogens are able to

reduce vegetative growth of a pioneer dune grass Am-

mophila arenaria (Marram grass; Va

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