Journal of Experimental Botany, Vol. 64, No. 5, pp. 1295–1303, 2013
doi:10.1093/jxb/ert007 Advance Access publication 18 January, 2013
Review paper
Soil abiotic factors influence interactions between
belowground herbivores and plant roots
Matthias Erb1,* and Jing Lu1,2
1
Root–Herbivore Interactions Group, Max Planck Institute for Chemical Ecology, Hans-Knoell-Str. 8, D-07745 Jena, Germany
Department of Biochemistry, Max Planck Institute for Chemical Ecology, Hans-Knoell-Str. 8, D-07745 Jena, Germany
2
* To whom correspondence should be addressed. E-mail: [email protected]
Received 8 July 2012; Revised 31 December 2012; Accepted 2 January 2013
Abstract
Root herbivores are important ecosystem drivers and agricultural pests, and, possibly as a consequence, plants protect their roots using a variety of defensive strategies. One aspect that distinguishes belowground from aboveground
plant–insect interactions is that roots are constantly exposed to a set of soil-specific abiotic factors. These factors
can profoundly influence root resistance, and, consequently, the outcome of the interaction with belowground feeders. In this review, we synthesize the current literature on the impact of soil moisture, nutrients, and texture on root–
herbivore interactions. We show that soil abiotic factors influence the interaction by modulating herbivore abundance
and behaviour, root growth and resistance, beneficial microorganisms, as well as natural enemies of the herbivores.
We suggest that abiotic heterogeneity may explain the high variability that is often encountered in root–herbivore
systems. We also propose that under abiotic stress, the relative fitness value of the roots and the potential negative
impact of herbivory increases, which may lead to a higher defensive investment and an increased recruitment of beneficial microorganisms by the plant. At the same time, both root-feeding herbivores and natural enemies are likely to
decrease in abundance under extreme environmental conditions, leading to a context- and species-specific impact
on plant fitness. Only by using tightly controlled experiments that include soil abiotic heterogeneity will it be possible
to understand the impact of root feeders on an ecosystem scale and to develop predictive models for pest occurrence
and impact.
Key words: Drought, induced resistance, moisture, plant immunity, root herbivores, soil texture.
Introduction
In their natural environment, plants encounter a diversity
of enemies, many of which have specialized to feed on specific plant tissues. Belowground herbivores in particular
are among the most damaging and dangerous pests as they
interrupt water and nutrient uptake as well as plant stability
by destroying parts of the root system (Hunter, 2001). The
impact of root-feeding insects on plant fitness is illustrated by
a recent meta-analysis that documents an average reduction
of 15% of plant reproductive output in the presence of root
feeders (Zvereva and Kozlov, 2012).
Recent research also demonstrates that plants possess
the capacity to defend themselves against root-feeding
insects (Van Der Putten, 2003); just as the leaves do, roots
produce a variety of toxic and repellent compounds that
fend off belowground attackers (Rasmann et al., 2011b;
Robert et al., 2012b). Furthermore, plants react dynamically to root attack: upon infestation, roots start producing specific blends of non-volatile and volatile secondary
compounds that are likely to increase the plant’s defensive capacity (Neveu et al., 2002; Kaplan et al., 2008).
Interestingly, roots typically do not show a strong jasmonate burst upon wounding, and it is possible that different regulatory mechanisms govern root and leaf responses
(Erb et al., 2012).
© The Author [2013]. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved.
For permissions, please email: [email protected]
1296 | Erb and Lu
A potentially important driver of belowground plant–
herbivore interactions is soil abiotic conditions: roots are in
constant contact with the soil, and a significant part of the
root structure and metabolism is adapted to deal with the
dynamic and heterogeneous environment below ground. For
instance, roots can sense moisture gradients to find moist
soil layers and perceive a lack or excess of water (Takahashi
and Scott, 1993); specialized root structures are formed to
exploit nutrient-rich patches (Beeckman and Friml, 2010;
Johnson et al., 2010a); and mechanosensing enables roots
to adjust their growth to circumvent impenetrable obstacles (Monshausen and Gilroy, 2009). Depending on the
abiotic environment, roots also adjust their interactions
with microbial mutualists and antagonists: mycorrhizal
colonization, for example, is favoured in phosphorus-limited environments (Jasper and Davy, 1993), and beneficial
microbes may be recruited specifically in times of need (Yi
et al., 2011).
Recent studies indicate strong effects of abiotic parameters
on root pest occurrence (Li et al., 2007a; Johnson et al., 2011).
However, how exactly do abiotic factors shape the interaction
between plant roots and root-feeding insects? Do plants balance their investment in growth and defence below ground,
depending on the soil environment? Also, how does abiotic
stress influence the impact of root herbivores on plant fitness?
These are the major questions that we address in this review.
Recent literature on the influence of soil abiotic factors on
root defences is discussed to complement two excellent classical reviews about the influence of soil abiotic factors on root
herbivore behaviour (Brown and Gange, 1990; Villani and
Wright, 1990). Our analysis focuses specifically on soil moisture, texture, and nutrient availability as important factors
that determine the outcome of root–herbivore interactions.
Although pH and temperature influence root herbivores as
well (Davis et al., 1996; Li et al., 2007b), they are discussed
only briefly. Rather than giving an exhaustive overview of
the available literature, we extrapolate current knowledge to
Quantitative aspects and optimal defensive
strategies
Abiotic factors can influence root–herbivore interactions on
several levels of complexity (Fig. 1A). First, the abiotic soil
environment can directly influence the abundance and distribution of belowground insects (Hoback et al., 2002; Johnson
et al., 2010a; Lepage et al., 2012). Soil drying, for example,
prompts many root feeders to move down to deeper layers of
the rhizosphere (Villani and Wright, 1988). Secondly, abiotic
factors can indirectly influence root feeders. For instance,
changes in root physiology and metabolism following abiotic
stress (Gao et al., 2007) may lead to changes in the nutritional quality and defence capacity of the roots. Abiotic factors may also influence the biotic environment that plants
and herbivores encounter (Fierer and Jackson, 2006), including, for example, natural enemies that may reduce herbivore
pressure.
Abiotic conditions influence plant–environment interactions in a quantitative manner (Fig. 1B). Soil moisture,
for instance, can range from flooding to complete dryness.
Overall, extreme conditions are likely to reduce both herbivore and plant fitness, unless the organisms are specifically adapted to thrive under these circumstances. In many
cases, however, abiotic conditions fluctuate around levels
that are within the range of physiological compensation for
both plants and insects (Fig. 1B). Even though the abiotic
changes may be subtle in this case, they may still strongly
influence the outcome of plant–herbivore interactions, and
we propose that understanding their impact may help to
explain some of the variability that is often observed in
studies involving root herbivores (Blossey and Hunt-Joshi,
2003; Erb et al., 2011).
(B)
Abiotic soil
conditions
Other soil
biota
Adaptive range
Root stress
Herbivore stress
Influence
(A)
1. Direct
predict general outcome patterns and identify major open
questions that will need to be addressed in the future.
3. Tripartite
Herbivore
Roots
2. Indirect
Root-herbivore
interactions
Abiotic condition
Fig. 1. Abiotic soil conditions affect root–herbivore interactions via several major routes. (A) Interactions are affected by direct influences
on herbivore behaviour and fitness (1), indirect influences of changes in plant metabolism and defences (2), and tripartite interactions
caused by changes in the soil biotic community (3). (B) The magnitude of the abiotic condition determines the severity of stress and the
impact of root–herbivore interactions. Both very low and very high levels of abiotic conditions can cause detrimental stress to roots and
herbivores. Within the physiological adaptation range, indirect interactions can be expected to be influenced most strongly, as the plants
reprogramme their metabolism to adjust to the environmental conditions.
Abiotic factors and root–herbivore interactions | 1297
Abiotic conditions may also alter the relative fitness value
of roots (Rasmann et al., 2011a), and, consequently, the
defence patterns that plants should employ to defend their
belowground organs. Water and nutrient limitation, for
example, can dramatically increase the importance of individual roots: under low stress conditions, plants can tolerate
the loss of a significant part of their root system without
suffering any negative consequences (Erb et al., 2009). The
situation dramatically worsens when the whole root system is
needed to acquire sufficient resources from the soil, as a relatively minor loss of absorptive tissue can already ‘tip the balance’ and lead to growth depression (Dunn and Frommelt,
1998). Because of the filamentous nature of roots, tissue loss
caused by herbivory is, in many cases, greater than the actual
amount of ingested tissue: if a root is severed by a belowground feeder, all the detached part is lost to the plant. Such
effects may amplify the loss of absorptive surface and further reduce plant performance under limiting soil conditions.
Following the optimal defence hypothesis (McKey, 1974),
plants should therefore protect their roots more strongly
under abiotic stress (Fig. 2). As an alternative strategy,
plants may invest more energy in root growth, which may
increase their tolerance to both stress and herbivory. The
interaction between abiotic stress and root herbivore tolerance is illustrated by a comparative study on root regrowth
and yield in 12 different maize genotypes: root regrowth in
plants attacked by Diabrotica virgifera improved yield under
low soil moisture, but not when enough water was available (Gray and Steffey, 1998). The fact that higher biomass
production can reduce the impact of both biotic and abiotic factors is specific to belowground tissues and may lead
to altered outcomes of growth/defence trade-offs compared
with the leaves. The hypothetical strategies as depicted in
Fig. 2 remain to be tested, but, as discussed below, evidence
is accumulating that at least some abiotic stresses increase
the defensive investment of roots.
Drought accentuates the impact of root
herbivory on plant fitness
Water limitation is a common feature of many natural and
agricultural systems, and reduced soil moisture can be an
important factor of root–herbivore interactions. Drought
stress can affect root-feeding insects directly (Villani and
Wright, 1990). Eggs of the clover root weevil Sitona lepidus
and the cabbage maggot Delia radicum, for instance, have
reduced hatching rates under drought conditions (Johnson
et al., 2010a; Lepage et al., 2012). It can therefore be expected
that water stress early in the season will reduce the overall
root herbivore load for plants. However, once herbivores have
established on the plant, they are likely to be less affected by
drought because (i) they can derive moisture from the root
system and (ii) they can move into deeper soil layers as drying sets in (Villani and Wright, 1988). The latter behavioural
adaptation may impact the interaction with plants, as deeper
rooting species and individual roots that have penetrated
the soil more deeply will be at an increased risk of attack,
while shallow roots will be less affected. It remains to be
determined whether plants alter the spatial distribution of
defences in anticipation of drought-induced movement of
root herbivores.
It is well known how profoundly plants adapt their metabolism to reduced soil water contents: as soon as roots sense
a reduction in soil moisture, they deploy systemic signals to
close stomata above ground, and the whole metabolism is
reprogrammed to respond appropriately to the stress conditions (Shao et al., 2009). Abscisic acid (ABA) signalling in
particular is important in plant adaptations to water stress
(Wilkinson and Davies, 2002; Chaves et al., 2003; Seki et al.,
2007). ABA has also been found to be a positive regulator of
insect resistance in Arabidopsis thaliana and tomato (Thaler
and Bostock, 2004; Monshausen and Gilroy, 2009), and it is
therefore possible that a plant’s drought stress response also
Defensive strategy
B
C
Root defensive
investment
Abiotic stress level
D
Relative
root value
Root growth
investment
Effect size
Effect size
A
Growth strategy
Root growth
investment
Relative root
value
Root defensive
investment
Abiotic stress level
Fig. 2. General predictive model of the effect of abiotic stress on root defences and growth in plants with contrasting strategies. (A)
Under low abiotic stress, the relative value of the roots is low, and the defensive investment is normal. (B) As the stress increases,
the root value increases, and plants may invest more energy in defences to protect roots. (C) As the stress leads to severe resource
limitation, the defensive investment is minimized to sustain basic metabolic functions. (D) Alternatively, plants may invest more energy in
root growth instead of defence, which would improve their tolerance against both herbivores and abiotic stress. Root-specific trade-offs
between the two strategies are likely to occur.
1298 | Erb and Lu
increases root resistance. One study documented increased
concentrations of glucosinolates in water-stressed turnip
(Brassica rapa) (Zhang et al., 2008), lending support to the
hypothesis that roots increase their defences under drought
stress. Few other studies have specifically measured the impact
of water stress on root defences, but a number of studies have
investigated systemic changes of defensive metabolites and
resistance in the leaves (Richardson and Bacon, 1993; Huberty
and Denno, 2004; Gutbrodt et al., 2011). Although it is difficult to extrapolate aboveground patterns to belowground
tissues (Erb et al., 2012), this body of literature illustrates the
potential of soil abiotic factors to determine the outcome of
plant–insect interactions via changes in host–plant resistance.
In general, drought stress has been found to increase the
negative impact of root feeders on plant fitness (Dunn and
Frommelt, 1998; Blossey and Hunt-Joshi, 2003). It remains
to be determined whether plants suffer more from root
removal despite or because of the absence of an increase
in plant resistance under these conditions. Water stress not
only accentuates the negative effects on plant yield, but can
also lead to negative effects of other herbivores that feed on
the plant: in maize, the growth of leaf feeders is reduced by
D. virgifera root infestation under water-limiting conditions,
but not when the plants are well watered (Erb et al., 2011).
The modulation of plant-mediated interactions of different
herbivores by abiotic factors adds another layer of complexity to the studied systems (Soler et al., 2012). However, it
remains to be determined whether this type of effect is relevant for the plant per se by altering fitness traits.
respirative oxygen loss (Soukup et al., 2007) and start producing roots that obtain oxygen through specialized aerenchyma (Laan et al., 1989). To date, little is known about the
effect of flooding on root resistance. The need to produce
new root tissue may lead to resource trade-offs and thereby
reduce defensive investment. On the other hand, the increase
in root lignification (Smaoui et al., 2011) and induced ethylene signalling (Hattori et al., 2011) may lead to augmented
root resistance (Johnson et al., 2010b), not so much as an
adaptation to changes in herbivore pressure, but as a secondary reaction to induced flooding tolerance. Unfortunately,
it remains experimentally challenging to assess the effect of
flooding on root resistance because of the direct effects of the
flooding event on herbivore fitness and behaviour. One study
investigated the impact of flooding on the susceptibility of
Swingle citrumelo to D. abbreviatus by infesting the plants by
submerging the roots and redraining them before herbivore
infestation. In this case, and in contrast to what was observed
in experiments with simultaneous flooding and infestation
(Li et al., 2007b; Martin et al., 2011), the roots were more
susceptible to the weevil larvae, indicating that flooding may
lead to a reduction in resistance (Li et al., 2006). In the future,
it seems important to understand whether anoxic soil conditions reduce root resistance in other plant species as well.
Understanding how the defensive potential of roots is modulated by flooding and genetic adaptation to this type of abiotic stress would also shed light on the hypotheses (i) that
flooding-tolerant plants invest less in root defences because
they grow in a largely ‘enemy-free’ space; and (ii) that insect
herbivores feeding in flooded environments benefit from the
lower root resistance.
Flooding reduces herbivore pressure
Excessive soil moisture following heavy rainfall can lead to
an anoxic soil environment. The absence of oxygen is detrimental for many root herbivores: D. virgifera larvae, for
example, cannot survive more than 24 h in a flooded environment (Hoback et al., 2002). It can therefore be expected that
prolonged flooding will reduce root herbivore pressure significantly. In accordance with this prediction, several studies on
the root herbivore Diaprepes abbreviatus feeding on Swingle
citrumelo found that the larvae suffered from a reduction of
growth and survival in flooded environments (Li et al., 2007b;
Martin et al., 2011). However, some root-feeding herbivores have specifically adapted to flooding: larvae of the rice
water weevil Lissorhoptrus oryzophilus, for example, feed on
rice roots below the water line and obtain oxygen through
the plant’s aerenchyma (Zhang et al., 2006). The rice water
weevil has moved from wild Cyperaceae and Poaceae to feed
on rice and is currently invading paddy environments across
the globe (Quisenberry and Heinrichs, 1998). Overall, it can
therefore be expected that flooding will, in the short term,
reduce root herbivore pressure for plants, but, if high moisture and low oxygen levels persist, adapted root feeders may
appear and threaten flooding-tolerant plants.
Anoxic soil conditions also trigger a pronounced response
in plant roots. Mediated largely by ethylene and ABA, flooding-tolerant plants enforce their apoplastic barriers to reduce
Organic matter and nutrients—does
deficiency increase plant defence?
In contrast to other abiotic factors, the availability of nutrients and soil organic matter is unlikely to impact root herbivores directly, as they obtain all of their essential dietary
constituents from the roots they feed on. Plants, on the other
hand, depend directly on the supply of essential elements
from the soil matrix, and virtually every aspect of plant life is
influenced by nutrient availability and uptake. In this context,
organic matter is important as it has a strong indirect impact
on the availability of soil nutrients by improving microbial
activity and retaining accessible nutrients.
Aboveground plant defences are well known to be modulated by soil nutrient supply. Nitrogen (N) limitation has been
shown to increase plant defensive investment in the leaves of
Zea mays and Gossypium hirsutum (Schmelz et al., 2003; Chen
et al., 2008), while neutral or negative effects were found in
Solanum lycopersicum (Stout et al., 1998) and Nicotiana attenuata (Baldwin and Hamilton, 2000). Potassium (K) deficiency
was shown to increase jasmonate signalling and glucosinolate
production in A. thaliana (Troufflard et al., 2010), while phosphorus (P) supply did not influence defences in Salvia officinalis and Pinus pinaster (Nell et al., 2009; Sampedro et al.,
2009). Are root defences affected in the same manner? From
Abiotic factors and root–herbivore interactions | 1299
an adaptive point of view, it can be expected that, similarly
to drought stress, the value of roots increases as resources
become scarce, which may lead to a more pronounced defensive investment in existing tissues. To date, few studies are
available to validate this prediction. Hol (2011) reviewed
studies on the influence of nutrient supply on pyrrolizidine
alkaloid (PA) concentrations in Senecio spp., and concluded
that overall, NPK fertilization reduces PA production in the
roots. Also, the application of nitrogen fertilizer tended to
increase L. oryzophilus populations in rice, even though plant
tolerance remained unaffected (Way et al., 2006). Clearly, further studies on other plant systems are needed to understand
how soil nutrient regimes affect root–herbivore interactions.
We hypothesize that, in general, root defences and resistance
should increase under low nutrient conditions.
Soil structure influences larval movement
The structural matrix that plants and herbivores encounter
below ground is not only an important determinant of nutrient availability and water retention, but influences both trophic
levels directly. Root herbivores in particular show pronounced
changes in mobility depending on bulk density and soil type
(Strnad and Bergman, 1987; Ellsbury et al., 1994; Pacchioli
and Hower, 2004). The magnitude of herbivore mobility again
determines whether herbivores choose between different host
plants, and whether they optimize their foraging strategy within
the root system. Diabrotica virgifera, for example, has been
shown in the laboratory to be able to use plant volatile compounds to select suitable host plants (Robert et al., 2012a), and
defensive metabolites to optimize its foraging pattern (Robert
et al., 2012b). If the soil structure favours movement, it can be
expected that D. virgifera will be able to employ these strategies relatively easily, while, under more difficult conditions,
larvae are more likely to limit their foraging range (Hibbard
et al., 2003). This aspect again has direct implications for the
success of plant defensive strategies: any defence aiming at
deterring herbivory will fail if the herbivore is unlikely to move
away from the plant due to environmentally imposed immobility. Also, selective defensive investment to protect the more
valuable belowground tissues may be ineffective as the risk of
attack of single tissues becomes unpredictable.
Do plants adjust their root defences depending on the soil
structure? It is well documented that roots have mechanosensors that enable them to bend if they encounter a non-penetrable soil layer. However, it has not been explored in detail
to what extent soil structure affects plant defences. Given that
root growth is more costly in dense soils (MacEwan et al.,
2010), the relative value of roots for the plant should increase,
which again should increase the plant’s defensive investment.
Contrary to this prediction, a study with woodland tobacco
(Nicotiana sylvestris) documents that pot-bound root systems
no longer respond to leaf induction and do not increase nicotine biosynthesis (Baldwin, 1988). However, Nicotiana spp.
are not typically threatened by insect root herbivores, and it
remains to be investigated whether plants that actively defend
their roots show a different pattern.
Changes in soil structure such as the moisture-dependent
swelling and shrinking of soil particles and the formation
of surface cracks can also directly impact root integrity. In
extreme cases, roots may be mechanically damaged by these
changes, which again may lead to an induction of defences
and resistance. In young maize seedlings, it was found that
mechanical damage is enough to trigger the production
of volatile organic compounds (Erb et al., 2012). From an
adaptive point of view, it may therefore be advantageous for
a plant to increase local resistance of broken roots: at least
some root herbivores prefer to oviposit and move within open
spaces in the soil (Vernon, 1979), and cracks in the soil surface may increase the risk of herbivore attack at this particular location.
Tritrophic and tripartite effects
As depicted in Fig. 1, soil abiotic conditions may also influence root–herbivore interactions by changing the distribution
and abundance of soil microorganisms and natural enemies
of the herbivores. In this section, we discuss a number of
examples that illustrate the diversity of possible outcomes of
tritrophic and tripartite interactions as they are modulated by
soil abiotic factors.
Upon root herbivore attack, plants start producing volatile organic compounds that diffuse through the soil and can
be used by entomopathogenic nematodes to locate their prey
(Rasmann et al., 2005). This type of tritrophic interaction
is strongly affected by abiotic factors in at least three ways:
first, the inducibility of the volatile signals may be affected
by nutrient availability (Ibrahim et al., 2008) and water status (Gouinguene and Turlings, 2002). Secondly, the diffusion
of volatiles through the soil is influenced by soil moisture:
both high and low water levels impair diffusion (Hiltpold and
Turlings, 2008). Thirdly, the activity and movement of the
entomopathogenic nematodes are influenced by soil structure (Schroeder and Beavers, 1987) and moisture (Grant and
Villani, 2003). Overall, it appears that attracting entomopathogenic nematodes is most effective in humid, well-structured
soils, but may not function under more extreme conditions.
Soil microorganisms can affect herbivores directly by acting as entomopathogens, but can also indirectly influence
plant defences, be it as beneficial mutualists (Zamioudis and
Pieterse, 2012) or as antagonists (Millet et al., 2010). The
composition of microorganisms in the soil is again significantly affected by many abiotic parameters including moisture, organic matter content, and pH (Fierer and Jackson,
2006). Plants may also manage their microbial community
to fit their environment. Mycorrhizal fungi are a prominent
example of this notion, as plants only allow an interaction
to occur when they need to improve their capacity for nutrient acquisition (Breuillin et al., 2010). Simulated leaf attack
of Medicago truncatula was also shown to stimulate colonization of the roots by Glomus intraradices (Landgraf et al.,
2012), and whitefly infestation facilitates rhizobium interactions (Yang et al., 2011), both of which may help the plant to
tolerate the leaf attack. Similar effects can be expected below
1300 | Erb and Lu
ground: resistance of Taraxacum officinale plants against the
black vine weevil Otiorhynchus sulcatus, for example, was
shown to increase dramatically in the presence of the arbuscular mycorrhizal fungus (AMF) Glomus mosseae (Gange
et al., 1994). In this context, it should be noted that AMF
effects on plant resistance against insects varies substantially
depending on the feeding mode and degree of specialization
of the herbivore (Koricheva et al., 2009). In general, however,
as plants may acquire beneficial microbes under stress conditions, and because at least some of them can be expected to
increase plant resistance, we hypothesize that abiotic stress
increases root defences via tripartite interactions, as long as
the microbial populations are not by themselves affected by
the adverse environment.
conditions, this may not necessarily be an appropriate
choice, as root herbivore growth may be affected by nutritional changes in the roots that are not related to defensive
patterns. We suggest therefore that as an ecologically and
agriculturally relevant measure, consumed root biomass
should be measured to assess the outcome of the interaction for the plant.
•• Although root herbivory is a common and frequent threat
to many plants, not all species have evolved in an environment that is colonized by root feeders. Short-lived annuals
and desert plants, for example, are unlikely to encounter root feeders in nature and may therefore not display a
meaningful behaviour when infested with such herbivores.
We therefore propose that the natural history of the investigated plant–insect system should be considered when
designing experiments.
Into the unknown—a brief research agenda
Our current knowledge on the role of abiotic factors in root–
herbivore interactions is very limited, despite the obvious
importance of this subject for the research field. One reason
for this may be the considerable challenges that are associated
with performing experiments on root herbivores as well as the
difficulty in disentangling direct from indirect effects (Fig. 1).
Here, we suggest a number of approaches that may help to
tackle the most pressing questions discussed in this article.
•• A major issue when investigating soil abiotic factors is that
they may influence both the herbivores and the plant, making it difficult to determine the actual driver of the observed
effects. This problem has been overcome in plant–mycorrhiza interactions by employing split-root systems: by separating the roots of a plant into two halves, one side of the
root system can be subjected to a particular stress, while
the systemic side can remain under control conditions. This
procedure enables the elimination of direct effects of the
abiotic factor on the herbivore.
•• A drawback of the above procedure is that only systemic
effects can be investigated. Another method to assess the
expression of constitutive and induced root defences may
be to substitute the herbivore with treatment causing
mechanical damage. Piercing roots with a needle or a fine
cork-borer can trigger a defensive response below ground
(Erb et al., 2012). Using herbivore elicitors may be an even
more reliable way to mimic herbivory (Schmelz et al., 2009).
Defences can then be measured and enable first conclusions
about the impact of a particular abiotic stress.
•• One prediction of this review is that there may be specific
growth/defence trade-offs in roots that could become important under limiting abiotic conditions. Experiments should
therefore involve the quantification of defences and resistance together with measures of root growth. Novel imaging
methods such as X-ray tomography (Johnson et al., 2007)
may make it possible to integrate this kind of parameter in
the future. As a rough proxy, measuring root branching and
mass in a destructive manner may be employed.
•• In many studies, herbivore growth is taken as a measure
of plant resistance. When dealing with variable abiotic
Major hypotheses and conclusions
Abiotic factors have a strong impact on root–herbivore interactions by influencing herbivore abundance, plant defence,
and growth, as well as tritrophic and tripartite interactions.
To date, few of these aspects have been researched in detail,
making it difficult to predict how environmental change and
variability will impact root-feeding insects. From the current literature, we propose several hypotheses that could be
tested in the future to understand the role of abiotic factors
in belowground plant–insect interactions.
(i) Soil abiotic stress increases the fitness value of individual
roots for the plant.
(ii) Severe stress reduces the probability that roots encounter
herbivores or natural enemies, but increases their interaction
with beneficial microorganisms.
(iii)Soil abiotic stress increases the negative impact of root
removal by herbivores on plant fitness.
(iv)Moderate soil abiotic stress increases the investment of
plants in root resistance.
(v) Plants that respond to abiotic stress by increasing root
growth display trade-offs with defences.
Already from the above hypotheses, it becomes clear that
the final outcome, i.e. the net effect of an abiotic factor on
the impact of root herbivores on plant fitness, will be highly
context dependent. In this review, we have highlighted six
major factors that are likely to determine the strength and
direction of the final outcome of the interaction: (i) the
severity of the abiotic stress; (ii) changes in density of root
herbivores; (iii) changes in density of natural enemies; (iv)
changes in the soil microbial community; (v) the plasticity
of the plant’s response to the abiotic factors; and (vi) the
susceptibility of the herbivore to the responses induced by
abiotic stress. Only if all these aspects are understood in
detail can predictions be made on how abiotic factors will
influence plant–insect interactions on an ecosystem scale, be
it to elucidate natural distribution patterns or to model pest
occurrence in agriculture.
Abiotic factors and root–herbivore interactions | 1301
Acknowledgements
We thank Mike Roberts for the invitation to contribute to
this special issue. Three anonymous reviewers provided helpful comments on an earlier version of this manuscript. The
work of ME is supported by a Marie Curie Intra European
Fellowship (grant no. 273107).
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