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Introduction

  1. Top of page
  2. Introduction
  3. Consequences of root-feeding for plants
  4. Control of root-feeding insects
  5. Root defences
  6. Community-level effects of root-feeding insects and complex interactions
  7. Conclusions and future work
  8. Acknowledgement
  9. References

Data from diverse ecosystems indicate that more than 50% of net primary production is commonly allocated to below-ground plant parts (Coleman, 1976), and values for particular plant species approach 90% (Andersen, 1987). Root biomass can typically vary from under 300 g/m2 to over 4000 g/m2 of soil surface (Rickleffs, 1973) and, however, you look at it, that's a lot of biomass. Although the nutritional value of root tissue is generally lower than that of foliar tissue, we shouldn't be surprised that many species of herbivore, including insects, exploit the roots of plants. What is surprising, however, is the extreme paucity of information on the distribution, abundance and effects of root-feeding insects on plants in natural and managed systems. If we as entomologists were to use our peer-reviewed literature as an indication of the relative allocation by plants to foliage and roots, we would get a shockingly biased picture. Over the last 5 years, for example, Ecological Entomology (5 years) and Agricultural and Forest Entomology (1 year) have published a combined four articles on root-feeding insects in comparison to 288 articles on insects that feed on above-ground plant parts.

With this apparent bias in effort, it's little wonder that even basic information on the distribution and abundance of root-feeding insects is missing for most ecosystems (Morón-Ríos et al. 1997). Yet below-ground insect herbivores are known to influence the diversity of plant communities, the rate and direction of succession, competitive interactions among plants, their allocation to different functions, the susceptibility of plants to other herbivores and pathogens and, ultimately, the yield of agricultural and forest systems (below). This paper considers what we do know about the effects of root-feeding insects on plants, and where our major knowledge gaps remain. Its intent is to stimulate discussion and an increase in research efforts on the ecology and management of below-ground insect herbivores. For purposes of brevity, ‘root-feeding’ is used here as shorthand for consumption of all below-ground tissues, including roots, rhizomes and other storage organs.

Consequences of root-feeding for plants

  1. Top of page
  2. Introduction
  3. Consequences of root-feeding for plants
  4. Control of root-feeding insects
  5. Root defences
  6. Community-level effects of root-feeding insects and complex interactions
  7. Conclusions and future work
  8. Acknowledgement
  9. References

Removal of root tissue by insect herbivores can result in a diversity of responses in their host plants, varying from changes in root : shoot ratios, through changes in subsequent carbon and nitrogen allocation, to death of the plants. Of course, the effects of root herbivory on plants are not restricted to loss of root tissue. In mixed-grass prairie, for example, root-feeding can reduce annual net primary productivity by 16 times more than is actually consumed (Ingham & Detling, 1990). In both agricultural (Latin & Reed, 1985) and forest (Klepzig et al. 1996) systems, root-feeding insects can introduce plant pathogens that affect survival and yield.

There is no clear consensus as to whether loss of biomass from root or shoot tissue has the greatest deleterious effects on plant performance but, in at least one study, removal of root tissue had a greater effect on plant performance than did removal of shoot tissue (Reichman & Smith, 1991). Root herbivores may cause losses in protein from the tap root, a reduction in non-structural carbohydrate root reserves and, subsequently, plant mortality (Godfrey et al. 1987; Dintenfass & Brown, 1988a,1b). However, plants infested by root-feeding insects may also exhibit increases in root nitrogen content and a concomitant reduction in foliar N content, reflecting a redirection of nitrogen to the stronger sink (Steinger & Müller-Schärer, 1992). It would seem important that future studies direct attention to whether differences in experimental results (i.e. increases or decreases in root nitrogen content) reflect differences in the plants under study, the identity of the root herbivores, or other ecological variables. This is the kind of basic information that is still lacking.

It seems likely, however, that lumping all root-feeding insects together into a single functional group and expecting them to have similar effects on their host plants may be a considerable oversimplification. In the same way that plants respond differentially to attack by different species or guilds of insect herbivores above ground (Hunter, 2000a) so we should expect differential effects of below-ground herbivores on plant performance. This was aptly demonstrated by Steinger & Müller-Schärer, (1992), who found that root-feeding by the moth Agapeta zoegana on Centaurea maculosa seedlings had no effect on shoot or root mass. By contrast, feeding by the weevil Cyphocleomus achates on the same plant greatly reduced shoot biomass.

At least some plants can tolerate significant levels of root herbivory, even under water stress (Dunn & Frommelt, 1998), with compensatory growth replacing root biomass (Schmid et al. 1990). In legumes, there can be compensation for nodule damage by insect herbivores (Quinn & Hall, 1992), although the compensatory mechanisms may be insufficient to prevent reductions in the nitrogen concentrations of tissue. In the legume Medicago sativa, compensatory responses are strong and denodulated plants recover nodule number and nodule biomass within 15 and 22 days, respectively (Quinn & Hall, 1996). Indeed, many plants appear to be adept at re-growing lost root tissue and, as a side note, this may lead us to underestimate the impacts of below-ground herbivores. However, compensation for root loss is not without cost and compensatory root growth in response to below-ground herbivory may often occur at the expense of above-ground net primary production (Andersen, 1987). Losses in above-ground biomass appear to be a common response to root damage by insects. For example, root herbivory on white clover by Sitona flavescens reduces foliar biomass, total nitrogen and carbon contents, and impairs nitrogen fixation (Murray et al. 1996). Likewise, feeding by Cerotoma arcuata larvae on bean roots and nodules reduces plant growth and subsequent yield (Teixeira et al. 1996). As Goldson et al. (1988) point out, compensation is associated with increased respiration rates and depleted carbohydrate reserves within the plant as assimilates from shoot reserves are diverted to satisfy the increased demands of the root system. Moreover, even when vegetative recovery seems to be high, compensation for root damage does not necessarily mean that subsequent reproductive output, competitive ability and nutrient or water uptake will be as high as those of undamaged plants (Detling et al. 1980). At least some of the deleterious effects on plants of root damage are likely to be expressed indirectly through interactions with other organisms and the environment (see below).

Given that compensatory root growth may lead us to underestimate the densities and activities of root-feeding insects, we may be most likely to recognize their effects post mortem. For example, root-feeding insects are associated with pine seedling mortality in the south-eastern United States (Mitchell et al. 1991) and Eucalyptus seedling mortality in plantations in India (Nair & Varma, 1985). In a spectacular example, ghost moth caterpillars can cause up to 41% mortality in bush lupine stands in California (Strong et al. 1995) and appear to contribute to the long-term dynamics of lupine populations. However, entomopathogenic nematodes can greatly reduce populations of ghost moth caterpillars and the ultimate effect of root-feeding on bush lupine populations probably reflects complex interactions among many ecological players (Strong et al. 1996, 1999). Interestingly, the fecundity of bush lupines can take 3 years to respond to suppression of below-ground herbivory (Maron, 1998), suggesting that short-term experiments may again underestimate the impact of root-feeding insects on plant populations.

Unless root-feeding insects cause substantial crop mortality, or directly attack plant parts that are harvested for economic gain, their impacts on financial yield can be difficult to assess. Nonetheless, some root-feeding insects have been shown to have dramatic effects upon production systems. During the 1990s, black pine weevil, Otiorhynchus sulcatus, progressively became the most serious pest in European ornamental nursery stock and soft fruit production (Labuschagne, 1999). Larvae feed on both roots and crown and the devastating nature of the pest means that the threshold for control may be very low. Its pest status is exacerbated by life-history traits that include a wide range of alternative hosts (weeds and non-crop plants) and a fecundity of between 500 and 1200 eggs per female per season. Like many root-feeding pests, O. sulcatus is difficult to detect during the early stages of outbreak and its densities are hard to monitor. They are also difficult to detect before or during the transportation of soil or nursery stock.

Nodule-feeding insects that attack nitrogen-fixing legumes can also be serious pests. Although well-recognized as pests of pulse crops such as peas and beans (O'Keefe et al. 1984), they can also cause economic problems in other production systems. For example, low input grassland systems managed for grazing usually require nitrogen-fixing legumes such as clover (Murray & Clements, 1999) that are useful both as a nitrogen source for the soil and as forage for livestock. Many agricultural soils are also enriched by the planting of legumes as ‘green manure’ (P. F. Hendrix, personal communication). Weevils in the genus Sitona seem to be particularly important pests in such systems as a consequence of nodule feeding by young larvae and root-feeding by older larvae. In fact, Sitona lineatus, distributed throughout Europe and in the western United States, is responsible for serious losses in yield to both edible legumes and forage legumes (Jackson, 1920; Oschmann, 1984). Again, estimates of yield losses may often be underestimated because of the difficulties associated with measuring damage by larvae.

In addition to such well-known pests as corn rootworm and cabbage root fly, root-feeding insects influence many other production systems. These include the turf grass industry, where both yield and aesthetic quality affect economic value (Crutchfield & Potter, 1995), and apple, orchards where root-feeding aphids can reduce tree growth and the number and weight of fruit per tree (Brown et al. 1995). Given the ability of some below-ground herbivores to depress plant growth and reproduction, it is not surprising that they are often evaluated as potential biological control agents of weed pests (Müller-Schärer, 1991; Blossey, 1993; Sheppard et al. 1995; Harris & Clapperton, 1997; Schwarzlaender, 1997). In a well-studied example, control of Senecio jacobaea in California has been maintained over the long-term by the combined activities of a defoliating moth and a root-feeding flea beetle (Pemberton & Turner, 1990).

Control of root-feeding insects

  1. Top of page
  2. Introduction
  3. Consequences of root-feeding for plants
  4. Control of root-feeding insects
  5. Root defences
  6. Community-level effects of root-feeding insects and complex interactions
  7. Conclusions and future work
  8. Acknowledgement
  9. References

Control of root-feeding insects in production systems is hampered, in part, by the difficulties of detection and access. Simply put, it is difficult to know when intervention is required and even more difficult to target a substantial proportion of the pest population with the chosen method of control. Some measure of success against the black pine weevil has been achieved using glue-coated barriers and trap cropping with favoured plant species (Labuschagne, 1999). Biological control of this and other root pests using entomopathogenic nematodes may provide the most promise (Kakouli et al. 1997), given that they may be specific to the pest and can be applied through a variety of measures including irrigation systems. Entomopathogenic nematodes also appear to be important mortality agents in some natural systems (Strong et al. 1996, 1999), suggesting that their life-histories are well-suited for exploitation as agents of control.

The jury is still out on the effectiveness of general predators as biological control agents of root-feeding insects. Carabid ground beetles would appear to have significant potential as control agents, but their reported impact on pests such as the cabbage root fly (Hughes, 1959; Coaker & Williams, 1963) may have been overestimated (Finch & Elliot, 1999). Recent studies have indicated that the efficacy of beetle predators is directly related to the relative size of beetle and prey (Finch, 1996), which may aid in the selection of potential control agents. As studies by Finch & Elliott, (1999) make clear, beetle predators are much more effective when the life stages of the pest are directly accessible on the soil surface, and even thin layers of soil covering the prey items can prevent the successful suppression of prey populations. Of course, selection of appropriate generalist predators for biological control is predicated upon knowing what they consume and in what proportion. Prey-specific monoclonal antibodies appear to have considerable potential as indicators of diet breadth in generalists such as carabids (Harwood et al. 1999; Symondson & Glen, 1999). Once again, however, we are limited by a basic lack of knowledge of both pest and predator ecology.

Chemical control of root-feeding insects has been the most common intervention strategy. However, there are concerns with the safety of commonly used products such as Chlorpyrifos (Dursban), which provides only a few weeks of control in its standard formulation. The extended release formulation of Chlorpyrifos (suScon Green) lasts longer in the environment, but is more expensive and less likely to come into contact with individual root pests. Both formulations can kill natural enemies and other soil fauna.

Given that Bt-transgenic corn can release biologically active Bt into the rhizosphere in root exudates (Saxena et al. 1999), there exists the potential to develop transgenic crops modified specifically to defend themselves against root-feeding insects. Of course, the continuing controversy surrounding the development and use of genetically modified crops (Hunter, 2000b) may limit the exploitation of transgenic plants for use against root-feeding insects. Such crops would, however, solve the problem of access by ensuring contact between pest populations and the mechanism of control.

Cultural control methods also have potential to reduce economic losses imposed by below-ground insect herbivores (Potter et al. 1996). For example, seasonal draining of rice fields can reduce oviposition by rice water weevil (Hesler et al. 1992). Likewise, traditional plant breeding programmes may be able to select for crops that are either tolerant or resistant to damage by root-feeding insects. In one of the few studies to address the issue, Houle & Simard 1996) found that compensatory responses (tolerance) of willow plants to simulated root herbivory did not vary among willow genotypes. The apparent lack of genetic variation in tolerance to root herbivory requires further investigation, given that genetic variation for resistance has been observed in several other systems (Powell et al. 1983; Byers et al. 1996; Strong et al. 1996). Indeed, the entire issue of genetically based resistance and tolerance to below-ground herbivores requires much more exploration in combination with mechanistic studies of root defence.

Root defences

  1. Top of page
  2. Introduction
  3. Consequences of root-feeding for plants
  4. Control of root-feeding insects
  5. Root defences
  6. Community-level effects of root-feeding insects and complex interactions
  7. Conclusions and future work
  8. Acknowledgement
  9. References

One of the most striking gaps in our understanding of below-ground herbivory is the degree to which below-ground structures (roots, rhizomes, etc.) gain protection from herbivory through chemical defence. There is little doubt that some below-ground plant organs contain high concentrations of toxins (e.g. the potent alkaloids in the rhizomes of bloodroot, Sanguinaria canadensis). However, the standard bioassays and measurements of insect performance, so prevalent in studies of above-ground insect herbivory, are generally lacking in below-ground systems. For example, although the presence of phenylpropanoid-derived metabolites in some plant roots is well established (Graham, 1991), their effects on insect herbivores have received little attention. Likewise, fine roots of forest trees often contain astringent phenolics and their concentrations generally increase as soil fertility declines (Muller et al. 1989). However, the degree to which astringent phenolics deter root-feeding insects is presently unclear.

Studies of defence induction in roots are also in their infancy. Although both synthesis and concentrations of some plant defences are known to be high in roots (Baldwin, 1989; Tallamy & McCloud, 1991), comparatively little work has examined the effects of induced defences in roots on root-feeding insects. The few studies to date suggest that, as in above-ground tissues, defence induction in roots may be a common phenomenon. Grape (Vitis vinifera) roots can respond to attack by Phylloxera vastatrix aphids by producing a local necrotic zone around each aphid that isolates attackers from healthy tissue (Karban & Baldwin, 1997). Roots of wild parsnip, Pastinaca sativa, respond to damage by increases in their concentrations of furanocoumarins (Zangerl & Rutledge, 1996). In a compelling example, damage to spinach roots induces phytoecdysteroids (analogues of insect moulting hormones), whereas infection by fungal pathogens does not (Schmelz et al. 1998, 1999). Given that foliar concentrations of phytoecdysteroids are unaffected by root damage, this provides evidence of an evolved defence in spinach roots directed at below-ground insect herbivores.

However, the effects of insect herbivores on the induction of defences in roots may be complex. For example, damage by turnip root fly, Delia floralis, causes a linear increase in only one of 14 glucosinolates in swede roots. An apparent balance between increases in aromatic glucosinolates and decreases in aliphatic glucosinolates results in overall glucosinolate concentration being unaffected by root damage (Hopkins et al. 1998). There are, of course, methodological difficulties associated with assessing putative chemical defences and their effects on insect herbivores below ground. In vitro root culture techniques may prove useful in future studies of root defence against herbivores (Wu et al. 1999).

Community-level effects of root-feeding insects and complex interactions

  1. Top of page
  2. Introduction
  3. Consequences of root-feeding for plants
  4. Control of root-feeding insects
  5. Root defences
  6. Community-level effects of root-feeding insects and complex interactions
  7. Conclusions and future work
  8. Acknowledgement
  9. References

It would be naïve to expect that interactions between root-feeding insects and their host plants occur in isolation from other species in the community or are unaffected by interactions with the abiotic environment. Below-ground insect herbivores are members of complex food webs and participate in both community-level and ecosystem-level processes. Consequently, both biotic and abiotic forces interact with below-ground herbivory to dictate plant performance (Godfrey & Yeargan, 1985). For example, the effects of root-feeding on Vicia establishment vary with both soil fertility and levels of mycorrhizal infection (Ganade & Brown, 1997). Likewise, compensation by Centaurea maculosa for weevil herbivory on its roots is greatly compromised by nutrient deficiency (Steinger & Müller-Schärer (1992). In a fascinating multi-trophic interaction, fungal endophytes (Acremonium spp.) associated with fescue grasses increase the susceptibility of root-feeding Japanese beetle larvae to the entomopathogenic nematode Heterorhabditis bacteriophora (Grewal et al. 1995). Competition among plants can overwhelm the effect of root herbivory in some systems (Müller-Schärer, 1991), but not in others (Noetzold et al. 1997). It seems likely then that interactions among root feeding and other ecological factors will prove to be complex and context-dependent in many systems.

Studies by Val Brown and colleagues have been instrumental in highlighting the effects of below-ground herbivores on plant diversity. At the community level, insect herbivory below ground can reduce plant species richness and alter patterns of succession in European old fields (Brown & Gange, 1989). Specifically, root-feeding insects can accelerate succession by reducing forb persistence and colonization (Brown & Gange, 1992) with the application of soil insecticide increasing plant species richness, vegetative cover and plant size (Masters & Brown, 1997). In short-grass prairie, even infrequent outbreaks of insect herbivores below ground can have long-term effects on plant community dynamics and recovery from disturbance (Coffin et al. 1998). Of course, the effects of below-ground herbivory on plant biomass and species diversity can vary both seasonally and with the plant species under investigation (Wardle & Barker, 1997). At the ecosystem level, low levels of below-ground herbivory can increase nitrogen flux from plants to soil, increase soil microbial activity, and increase the rates of nitrogen recycling in grassland ecosystems (Bardgett et al. 1999). In tallgrass prairie, the emergence of annual cicadas can represent a significant flux of non-gaseous nitrogen from below-to above-ground (Callaham et al. 2000).

Mycorrhizae, as a result of their intimate associations with root systems, may influence feeding by below-ground herbivores by changing the quality or the quantity of root resources (Gange, 1999). If studies of root–insect herbivore interactions are relatively rare, those that consider mycorrhizae are positively endangered! The data that do exist suggest that colonization of plant roots by arbuscular mycorrhizae (AM) has a negative impact on root-feeding insects. For example, Gange et al. (1994) demonstrated that the survival and biomass of black pine weevil larvae feeding on the roots of Taraxacum officinale were halved by the presence of the mycorrhizal fungus Glomus mosseae. When Gange (1996) repeated the experiment using strawberry as a host-plant, root colonization by a single species of AM again reduced the performance of weevil larvae. However, when roots were colonized by two AM species simultaneously, the negative effects on the root-feeding insect disappeared. Extrapolating from a single study is dangerous, but it suggests that any resistance factor(s) conferred on roots by their association with mycorrhizae may be compromised if multiple infection takes place. Given that mycorrhizal colonization generally increases the biomass of roots (Smith & Read, 1997), their putative effects upon root resistance to herbivores is more likely to be mediated by changes in root quality than root quantity (Gange, 1999).

As studies of below-ground herbivory become more common, complex interactions among community members both above- and below-ground are likely to emerge. For example, foliage removal by a leaf-chewing insects can result in reduced mycorrhizal colonization of plant roots (Gehring & Whitham, 1991; Gange & Bower, 1997). Given that mycorrhizal colonization can confer resistance to root feeders (Gange et al. 1994; Gange, 1996), above-ground defoliation has the potential to increase the susceptibility of roots to their herbivores. However, most studies seem to suggest that the opposite is true; stem- and leaf-feeding insects appear to reduce the performance of root-feeding insects. For example, Moran & Whitham, (1990) demonstrated that leaf galling by aphids on Chenopodium can lead to a large reduction in the populations of root-feeding aphids. Conversely, below-ground damage by insect herbivores is generally thought to increase the quality of plant tissues for above-ground herbivores (Gange & Brown, 1989; Masters et al. 1993). These complex interactions between below- and above-ground herbivores are potentially very important. When we observe high densities of insect herbivores feeding upon the leaves and shoots of our agricultural and timber crops, we rarely consider the possibility that the severity of their depredations may result, in part, from high densities of root-feeding insects. Likewise, yield increases following the successful control of above-ground insect pests may be compromised by subsequent increases in the densities of root-feeding herbivores.

It may be early to speak of generalities when so few data are available, but the current consensus appears to be that the patterns described by Moran & Whitham, (1990) and Gange & Brown, (1989) may be common; above-ground herbivory has a negative effect on root-feeders, whereas below-ground herbivory has a positive effect on foliar feeders (Masters et al. 1993; Masters, 1999). The evidence for such contramensal interactions (Arthur & Mitchell, 1989) comes from both laboratory and field studies. For example, root-feeding aphid populations on Cardamine are significantly reduced in the presence of shoot-feeding aphids (Salt et al. 1996). Similarly, the growth rates of chafer larvae feeding upon the roots of Sonchus oleraceus are reduced when leaves are concurrently mined by Agromyzid larvae (Masters & Brown, 1992). By contrast, the pupal weights of leaf miners are higher in the presence of chafers. Other guilds of above-ground herbivores (leaf-chewers, phloem-feeders) also respond positively to chafer damage in this system (Masters, 1999) while simultaneously depressing chafer growth rates. Field experiments employing soil insecticides (Masters, 1995b; Masters & Brown, 1997) and artificial root damage (Foggo & Speight, 1993; Foggo et al. 1994) support the view that below-ground herbivores facilitate population growth of insect herbivores above ground.

Interactions between above- and below-ground herbivores appear to be mediated primarily by increases in soluble nitrogen and sugar contents in above-ground tissues (root-feeders increase foliage quality) and decreases in root biomass below-ground (aerial herbivores depress root growth) (Holland & Detling, 1990; Masters, 1995a). More detailed investigations of mechanism are, however, desperately needed in such systems, including the potential induction or suppression of defences (Seastedt et al. 1988; Karban & Baldwin, 1997) and the signalling pathways responsible for both defensive and ‘civilian’ plant responses to damage (Hunter, 2000a). Such investigations may help to explain why some studies do not conform to established patterns. For example, above-ground grazing by vertebrates can increase the densities of root-feeding insects (Roberts & Morton, 1985; Seastedt et al. 1988), and artificial defoliation of bunchgrass, Muhlenbergia quadridentata, has no effect on root-feeding Phyllophaga larvae in Mexico (Morón-Ríos et al. 1997). Given the importance of damage-specific signal cascades to the defensive response of plants (Hunter, 2000a), we should not be surprised that vertebrate grazing, artificial damage and foliar-feeding insects generate different responses by plants and their below-ground herbivores.

Conclusions and future work

  1. Top of page
  2. Introduction
  3. Consequences of root-feeding for plants
  4. Control of root-feeding insects
  5. Root defences
  6. Community-level effects of root-feeding insects and complex interactions
  7. Conclusions and future work
  8. Acknowledgement
  9. References

In terms of relative biomass and productivity, below-ground plant parts represent a substantial fraction of the resources available to terrestrial herbivores. In terms of relative effort by insect ecologists, root-feeding insects have been greatly understudied. There are several areas of endeavour that would appear to require considerable work. First, we need detailed mechanistic studies of root defences. How variable are the physical and chemical defences of roots? Do they have a significant impact upon the populations of root-feeding insects? What signalling pathways are expressed during the induction of root defences and how are they affected by environmental variables? Second, we need to explore genetic variation in the tolerance and resistance of plant roots to their insect herbivores. An understanding of that genetic variation, and the role of the environment in its expression, will allow us to better comprehend the evolution of root defences and the potential to select for resistant and tolerant crop varieties. Third, we should explore the potential of genetically modified crops with tissue-specific root defences against root-feeding insects. Problems of applying control measures below ground may make transgenic plants a suitable option for reducing the depredations of below-ground crop pests. Of course, a detailed understanding of rhizosphere ecology and impacts on non-target organisms will also be required. Fourth, increased exploitation of entomopathogenic nematodes as control agents of root-feeding insects should be explored. They appear to have dramatic impacts in both natural and managed systems and are of great potential benefit to biological control programmes. Finally, studies of root herbivore–mycorrhizal interactions are considerably improving our understanding of soil ecology and their number should be greatly increased.

Insect ecologists are not generally reluctant to get their hands dirty, and the paucity of studies of below-ground herbivores may reflect methodological difficulties rather than lack of interest. It might be time for the funding agencies to develop financial incentives to encourage researchers to solve methodological limitations and to redress the imbalance that currently favours research on insects above ground. In any case, we have clearly had our heads in the sand on the issue of root-feeding insects. Unfortunately, most of us appear to have had our eyes shut at the time.

References

  1. Top of page
  2. Introduction
  3. Consequences of root-feeding for plants
  4. Control of root-feeding insects
  5. Root defences
  6. Community-level effects of root-feeding insects and complex interactions
  7. Conclusions and future work
  8. Acknowledgement
  9. References
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