Review
Impacts of soil microbial communities
on exotic plant invasions
Inderjit1 and Wim H. van der Putten2,3
1
Centre for Environmental Management of Degraded Ecosystems (CEMDE), University of Delhi, Delhi 110007, India
2
Department of Terrestrial Ecology, Netherlands Institute of Ecology, P.O. Box 40, 6666 ZG Heteren, The Netherlands
3
Laboratory of Nematology, Wageningen University, P.O. Box 8123, 6700 ES Wageningen, The Netherlands
Soil communities can have profound effects on inva-
sions of ecosystems by exotic plant species. We propose
that there are three main pathways by which this can
happen. First, plant–soil feedback interactions in the
invaded range are neutral to positive, whereas native
plants predominantly suffer from negative soil feedback
effects. Second, exotic plants can manipulate local soil
biota by enhancing pathogen levels or disrupting com-
munities of root symbionts, while suffering less from
this than native plants. Third, exotic plants produce
allelochemicals toxic to native plants that cannot be
detoxified by local soil communities, or that become
more toxic following microbial conversion. We discuss
the need for integrating these three pathways in order to
further understand how soil communities influence exo-
tic plant invasions.
Soil biota, invasive species and plant communities
Invasive species are a major threat to community compo-
sition and ecosystem processes worldwide [1]. Recent stu-
dies on exotic plants have revealed a wide variety of plant–
soil interactions that might lead to enhanced plant inva-
siveness in the new range. There have been several reviews
on interactions between invasive exotic plants and soil
communities, which argue that these interactions have
been severely overlooked as a factor explaining plant
invasiveness [2–7]. Here, we review and synthesize infor-
mation on plant–soil community interactions and develop
a conceptual framework that will enhance our understand-
ing of how interactions and processes in the belowground
world might contribute to plant invasiveness. We identify
three major pathways of plant–soil community inter-
actions, each containing mechanistically different, but
conceptually similar types of interactions that might
promote plant invasiveness. These are: plant–soil feed-
backs in the non-native range, impact of exotic plants on
soil communities of the non-native range and responses of
naı̈ve soil communities to novel chemicals. Such knowledge
of plant–soil community interactions will be pivotal for
developing integrated approaches for counteracting the
negative impacts of invasive plants. Although soil harbors
a wide variety of micro- and macro-organisms, we focus on
soil microbial communities, because their interactions
with exotic plants have been studied most [8–10].
Soil microbial communities influence the establishment
of exotic plants in their new range, and contribute to
Corresponding author: Inderjit, (inderjit@cemde.du.ac.in).
512 0169-5347/$ – see front matter ß 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2010.06.006 Trends in Ecology and Evolution 25 (2010) 512–519
invasiveness [11–14]. Soil biota that are native in the
invaded range exert neutral or positive [15] feedbacks on
exotic plants (Box 1). These can enhance interspecific
competitiveness of the exotic plants, since many native
plant species are subject to negative feedback effects [16–
19]. The phenomenon whereby exotic plants are released
from specialist, or virulent enemies is called ‘Enemy
Release’ [20]. Exotic plants, however, are still exposed to
the local enemies of the new range [21,22]. These local
enemies might exert negative feedback effects on the exotic
plants, and this could suppress their invasiveness [22]. The
phenomenon that exotic species are controlled by enemies
that are natural in the invaded range is called ‘Biotic
Resistance’ [20]. Nevertheless, when exotic plants accumu-
late local pathogens while remaining less affected than the
native plant species, plant invasiveness might be enhanced
[23]. Similar effects have been shown for aboveground
viruses in exotic tussock grasses that invade Californian
grasslands. The viruses accumulate on the exotic grasses
and then spread to the surrounding native plants, where
they reduce native plant performance [24]. Finally, exotic
plants can exude chemicals that are novel to the local soil
communities. Non-adaptation could hamper the ability of
the naı̈ve soil microbes to deal with novel chemicals or the
microbes could transform innocuous novel chemicals into
toxic chemicals [25].
In order to enhance conceptual understanding of all
these different exotic plant–soil microorganism inter-
actions, we develop a framework that includes the various
types of interactions within the framework of the three
pathways and show how it will promote plant invasion
(Box 1).
Plant–soil feedbacks in the non-native range
The rhizosphere is the narrow zone of soil surrounding the
root in which the abundance and composition of microbial
population are influenced by the presence of roots or their
exudates [10]. Soil microbial communities that accumulate
in the rhizosphere of a specific plant can have positive or
negative feedback effects on the plant that cultivates them,
or on the offspring of that plant (Box 1). These feedback
effects are the net result of all positive and negative
influences emerging from the soil biota in that community.
Negative plant–soil feedback controls abundance, because
the plants will not be able to stay productive throughout
their lifetime [18], or their offspring will not be able to
establish close to the parents [26]. It will also promote
coexistence, as plants become less competitive towards
Review
Box 1. Plant–soil feedbacks and exotic plant invasion
Plants are in constant feedback interactions with soil pathogens,
root herbivores, symbionts, decomposers, carnivores and antago-
nists. The net effects of these interactions are conceptualized as
plant–soil feedback and are usually assessed by growing plants in
soil previously conditioned by individuals of the same plant species.
Plant–soil feedback interactions have a direct component, which
concerns the soil biota that interact intimately with living plant
roots, and indirect effects concerning soil organisms that decom-
pose exudates and dead plant tissues [8] (Figure I). Here, in order to
better understand how plant-soil feedback promotes invasiveness,
we extend the indirect effects, as most plant–soil interactions
change the competitiveness of the host plant, which ultimately
determines performance of individual species in plant communities.
In Figure I, direct plant–soil feedback interactions between soil biota
and host plants are depicted on the left side. On the right side,
effects of nutrients released from plant litter act indirectly, as they
must pass through a stage of decomposing dead plant tissues.
[(Box_1)TD$FIG]
Then, on the far right side of Figure I, another set of indirect
interactions is shown, concerning exotic plant-mediated changes in
Figure I. Direct and indirect effects in plant-soil feedback interactions and consequences for exotic plant invasions.
other species [2,11,27]. Positive feedback effects, on the
other hand, result in the dominance of plants, since
microbial symbionts and other growth-promoting soil
microorganisms intensify interspecific competition [11].
Positive plant–soil feedback will also enhance intraspecific
competition. Most feedback effects observed in nature so
far have been negative [11,17].
In a seminal study, Klironomos [16] compared the
plant–soil feedback effects of exotic, native dominant
and native rare plants in a Canadian grassland of old field
soil. Soil colonized by individuals of the same species
Trends in Ecology and Evolution Vol.25 No.9
soil chemistry, symbiotic mutualists, or accumulated local patho-
gens. All these factors may suppress the performance of native
plants, here represented as a wilted seedling. This indirect
suppression of native plants will enhance the competitiveness of
the exotic, thereby enhancing its invasive dominance. In Figure I, ‘+’
indicates a net positive feedback or impact and ‘ ’ a net negative
feedback. Direct effects of soil communities include (i) local soil
communities, including soil pathogens and root herbivores that
resist invasion [30], (ii) native soil biota, including plant growth
promoting rhizobacteria that can create a positive feedback [15], and
(iii) complete or partial release from enemies (such as fungi or
viruses) [21]. Indirect effects of soil communities contributing to the
invasion success of an exotic plant are (i) accumulation of native soil
pathogens in the presence of an exotic plant [23,34], (ii) disruption
of mutualistic associations between native mutualistic symbionts
and seedlings of native plants [41,44], (iii) degradation of innocuous
novel chemicals released by exotic plants into toxic by-products by
native soil microbes [25], and (iv) nutrient release from exotic litter
by decomposers [57,58,67].
suppressed the growth of rare plant species, but did not
affect or even enhanced the growth of native dominant and
exotic plants. This study clearly demonstrated the link
between negative soil feedback and plant abundance and
suggested that invasive exotic plants benefit from release
of soil-borne enemies.
The first study showing that plant–soil feedback of an
exotic plant was negative in its native range, but neutral to
positive in the non-native range was carried out by Rein-
hart and co-workers [28]. They investigated the invasion of
Prunus serotina, a tree species native to the USA but
513
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invasive in Europe. Biogeographical experiments in the
native and non-native ranges led to the suggestion that,
while soil microbial communities in the native range in the
USA kill seedlings of P. serotina, soil microbes in the non-
native range in Europe exert a neutral to slightly positive
feedback on seedling growth [28]. Recently, it has been
shown that P. serotina has not escaped all soil pathogens,
but it has escaped the most virulent species [29]. DNA-
sequencing-based studies such as this open up new ave-
nues for work on the identity of soil pathogens involved in
controlling plant abundance in the native range.
Callaway et al. [15] provided further evidence that local
soil microbial communities can promote the performance of
an invasive exotic plant through positive soil feedback.
They compared performance of Centaurea maculosa, a
Eurasian invader in northwestern USA, in soil collected
from the native (European) and non-native (North Amer-
ican) ranges. Whereas sterilization of soil from the non-
native range tended to decrease C. maculosa growth,
sterilization of soil from the native range improved its
growth. This suggested that in the native range, soil com-
munities control plant growth, whereas in the non-native
range the soil communities tend to enhance plant growth.
These benefits that exotic plants get from local soil
communities might not apply to every exotic plant and
they might not last forever. For example, Nijjer et al. [30]
showed that Sepium sebiferum, a woody invader in the
USA, experienced growth reduction in soil collected near
conspecifics (home soil) compared to heterospecifics (away
soil). Fungicides reduced this growth-reducing effect in
home soil, suggesting that this invader might generate
soil pathogen activity over time. A very recent study from
New Zealand [31] confirmed that invasive exotic plants
might develop negative soil feedback from the time of
introduction. Dietz et al. [31] compared 12 plant species
that have become introduced to New Zealand over the last
210 years. There was a clear correlation between length of
time since introduction and the strength of negative feed-
back: plant species that were introduced longest ago had
the strongest negative soil feedback. The mechanism of
this effect remains unexplained.
Ageratina adenophora, an aggressive subtropical Mex-
ican invader, is rapidly spreading in India and China.
Through glasshouse studies, Niu et al. [32] found that soil
microbial communities associated with native plants exert
a positive impact on A. adenophora and a negative impact
on native plants. Once the invader has established itself in
the non-native range, it increases the abundance of arbus-
cular mycorrhizal fungi in the soil, as well as an increase in
the abundance of fungi relative to bacteria. The induction
of this shift in soil microbial communities by A. adenophora
can facilitate its growth and suppress native plants. Prin-
gle et al. [33] proposed a conceptual framework to under-
stand the role of mycorrhizal symbioses in plant invasions.
These authors suggested that after an exotic plant has
established in its new range, it can influence or be influ-
enced by mycorrhizal symbioses specific to itself and to the
non-native soil. These changes can influence establish-
ment and survival of native plants.
Most studies that have examined plant–soil feedback
effects of exotic plants have focused on the very few exotic
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Trends in Ecology and Evolution Vol.25 No.9
plant species that did become invasive in their new range.
What we lack in testing the enemy release hypothesis are
negative controls. Negative controls can include exotic
plants that have not become invasive. If these plants are
also released from their natural enemies and if they do not
encounter biotic resistance from soil communities in their
new range, it means other factors must be preventing these
species from becoming invasive. Such examples should be
studied in relation to plant community interactions and
would be useful in order to place release from soil-borne
and aboveground enemies into a better perspective.
Impact of exotic plants on soil communities of
the non-native range
Exotic plants can accumulate local pathogens in their
rhizosphere, and this can suppress native plants. When
the exotic plants suffer relatively less from these local
pathogens than the native plants, pathogen accumulation
will provide the exotic plants with an indirect advantage
in competition with the natives (see Boxes 1 and 2).
This is known as the Accumulation of Local Pathogens
hypothesis [23]. While examining the invasion success of
Chromolaena odorata, a destructive tropical invader in
the Western Ghats of India, Mangla et al. [34] provided
empirical evidence supporting the accumulation of
local pathogens hypothesis. Rhizosphere soils of C. odorata
accumulate high concentrations of a generalist soil
pathogen, which suppresses native plant species, since
these are more sensitive to the pathogen than the invader
itself [34]. Interestingly, another study on C. odorata, this
time interacting with the native grass Panicum maximum
in South Africa, did not reveal accumulation of local
pathogen effects [35]. Therefore, the role of the accumu-
lation of local pathogens in enhancing plant invasiveness
appears to depend on the combination of invader and local
plant species examined and possibly also on the habitat
invaded by the exotic plant.
Arbuscular mycorrhizal fungi (AMF) is a common endo-
mycorrhizal association produced by phycomycetous fungi
and characterized by the development, within root cells, of
small branched structures called arbuscules [10]. Until
recently, it had been proposed that invasive exotic plants
could easily make use of AMF, because interactions with
these fungi had been assumed to be relatively non-specific
[36]. However, these mutualistic symbionts are probably
far less generalist than had been supposed previously [37].
This might explain why invasive exotic plants reveal a
range of effects on AMF [38]. It has been suggested that the
weedy nature of many invasive exotic plants is correlated
with lower mycorrhizal-dependence [39], but there are
relatively few examples of studies that actually test mycor-
rhizal effects on exotic plants. In a comparative study, the
mycorrhizal status of invasive exotic plants was found to
depend on the plant species with which the exotic species
co-occur and the habitat that they invade [40]. These
results suggest that the success of invasive exotic plants
depends on which mycorrhizal fungi are available.
The framework of the Accumulation of Local Pathogens
hypothesis [23] can be extended to include ‘suppression of
symbiotic mutualists’, since exotic plants can reduce the
mycorrhizal inoculum in the invaded soil. In this way,
Review
Box 2. Soil-borne communities and Ammophila arenaria invasion
Soil borne communities (nematodes and fungi) restrict the growth of
Ammophila arenaria in Europe, its native range [18]. Ammophila
arenaria is invasive in North America, South Africa, Southern
Australia and New Zealand. Specialist pathogenic nematodes are
absent in the introduced range [68]; however, the plant’s escape from
enemies appears to be only partial considering the negative soil
feedback it experiences in California [22]. In South Africa, Sporobulus
virginicus harbors pathogenic fungi in its rhizosphere, and these offer
biotic resistance to A. arenaria [21]. Water could also be a limiting
factor in South Africa, since water limitation makes A. arenaria less
invasive [69]. In the native range, nematodes are abundant in A.
arenaria soil. Van der Stoel et al. [70] found that negative plant–soil
feedback in the native range of the plant follows root colonization in
newly deposited sand and colonization of the young roots by
endoparasitic nematodes Heterodera arenaria and Pratylenchus spp.
[(Box_2)TD$FIG]
In order to understand invasiveness of A. arenaria in California
despite the local soil-borne biotic resistance, Eppinga et al. [23] built a
Figure I. Results of interactions between Ammophila arenaria and soil organisms for its control and abundance in the native and non-native ranges.
invasive exotic plants can indirectly reduce the growth of
native plants by reducing the abundance and diversity of
local AMF communities on which the natives depend. For
example, the effect of the non-mycorrhizal exotic invasive
forb Alliaria petiolata, on AMF [41] and ectomycorrhizal
fungi [42] has been studied in North America. AMF and
ectomycorrhizal fungi are both phylogenetically and func-
tionally distinct, and so might have different responses to A.
petiolata invasion [42]. The invasive plant indirectly inhibits
native tree regeneration by suppressing ectomycorrhizal
fungi on which native tree seedlings depend [41,42]. Call-
away et al. [43] found that A. petiolata suppressed root
colonization by AMF and ectomycorrhizal fungi, and certain
native mycorrhizal species in the non-native range. No
similar impacts were observed when A. petiolata was grown
in native soils. Indirect evidence suggested that inhibition of
non co-evolved AMF is due to specific flavonoid molecules
released by A. petiolata, whereas in the native range, AMF
may not have to be sensitive to these compounds [43].
However, studies on suppression of mycorrhizal fungi
should include more negative controls than thus far. For
example, by including habitats in the native range where
the exotic invader is not occurring naturally. Including such
treatments helps to determine if non-adapted mycorrhizal
fungi are sensitive or not to A. petiolata in its native range.
Trends in Ecology and Evolution Vol.25 No.9
Lotka–Volterra-based model [11] to analyze how interactions between
soil communities and exotic plants could explain the invasion success
of A. arenaria. Results from this model [23] suggested that in
California, A. arenaria accumulates local pathogens, which reduce
the invader to some extent, but which reduce the performance of
native plant species more profoundly. This led the model’s authors to
propose the ‘Accumulation of Local Pathogens’ hypothesis suggest-
ing that invasive plants may benefit indirectly from local soil
pathogens even when they experience negative soil feedback,
assuming that they are more tolerant of the local soil pathogens
than are the native plants. Empirical support for this hypothesis
comes from spill-over literature; for example, introduced tussock
grasses in California can enhance the abundance of local viruses that
in turn have more negative effects on native plants than on the
invaders [24]. Thus, A. arenaria invasion combines aspects of the
enemy release, biotic resistance and accumulation of local pathogens
hypotheses, as outlined in the scheme Figure I below.
Besides their effects on mycorrhizal fungi, exotic plants
can make use of other symbionts to change plant com-
munity composition and ecosystem development. For
example, the fungal endosymbiont Neotyphodium coeno-
phialum, associated with the non-native fescue grass
Lolium arundinaceum, slows down succession from grass-
land to forest [44]. Soil mutualists contribute to the inva-
sion success of Acacia longifolia, an invasive plant of
Portuguese coastal dunes [45]. This plant species increases
its aboveground biomass in low N soils due to heavy
nodulation resulting in symbiotic N fixation. Invasive exo-
tic plants can also reduce abundance and performance of
N-fixing microbes, such as was suggested based on sup-
pression of AM fungi. This will reduce growth of Acacia
species in Amaranthus viridis-invaded soil. Aqueous root
extract of Amaranthus viridis inhibited rhizobia develop-
ment [46], suggesting that the exotic plants can interfere
with the symbiotic relationships between the native pants
and their symbionts. This and other mechanisms of indir-
ect influencing of native plants by exotics operating
through symbioses other than mycorrhizal fungi have been
rarely explored. Nevertheless, considering the importance
of these symbioses, their altered activity has profound
importance as explanations of how exotic plants can
become invasive.
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Responses of naı̈ve soil communities to novel chemicals
Some exotic plant species produce chemicals that are novel
to native plants in the invaded range. These chemicals
could be phytotoxic to plants that are native in the invaded
range. Plant species native to the region from which the
exotic plants originated are less likely to be affected by
these chemicals probably due to a history of co-evolution
with the plant species producing them. This concept pro-
vides the basis for the Novel Weapons Hypothesis [47,48]
and the effects might also stretch to the microbial commu-
nities of the non-native range. The novel weapons hypoth-
esis is largely based on studies of the role of catechin in the
invasion success of Centaurea maculosa in North America
[47]. This interesting and intriguing concept is still heavily
debated because of the low phytotoxicity and poor recovery
of catechin from invaded soil [49–51]. Here, we focus on the
how novel chemicals influence microbial communities and
their functioning. This is an aspect that has received
relatively little attention.
Novel chemicals released from exotic plants might, or
might not be decomposed by soil biota from the non-native
range. It has been generally supposed that soil decomposer
organisms have relatively low specificity. However, recent
studies have suggested that leaf litter can be better decom-
posed by soil communities from under trees that have
produced the litter than when the litter has been collected
further away [52]. The same principle could apply to the
degradation of plant chemicals. However, empirical evi-
dence for this assumption is lacking. If soil microbes do not
degrade the novel chemicals well enough, the chemicals
might accumulate and reach toxic levels. In the native
range, soil microbes will have evolved with these com-
pounds, and so it is possible that microbial genotypes or
species capable of degrading the chemicals have been
selected. If that were true, there would be less need for
co-occurring plants in the native range to be tolerant of
these chemicals, as decomposition by the native soil
microbes prevents accumulation to toxic levels.
In a more than 50 year chronosequence study of A.
petiolata invasion, Lankau et al. [53] found that both the
production of glucosinolates by A. petiolata and the associ-
ated soil-mediated effects of this chemical decline with
time. Seeds of A. petiolata from 44 populations across
the selected range were planted in a common experimental
garden for three months to determine root glucosinolate
levels. Soil previously grown with A. petiolata for three
months was used to study the performance of three native
plants, Plantanus occidentalis, Juglans nigra and Quercus
rubra. All of the three native plants produced more bio-
mass in soil conditioned by A. petiolata that originated
from old invasion sites. Least biomass was produced in soil
conditioned by exotic populations from recently invaded
sites. Although evidence at the microbial level is lacking,
these results suggest there is selection acting on the soil
microbial communities resulting in enhanced capacity to
degrade the allelochemicals. Indirect evidence for the
degradation of glucosinolates in the non-native range is
provided in a study of the suppression of Platanus occi-
dentalis seedlings by non-native A. petiolata [54]. Allelo-
pathic suppression of P. occidentalis was observed only in
sterile soils, suggesting the possible degradation by the soil
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Trends in Ecology and Evolution Vol.25 No.9
community of glucosinolates exuded by A. petiolata [54]. It
is therefore possible that soil microbial communities from
the non-native range might start degrading the novel
chemicals produced by exotic plants, thereby reducing
their invasive potential over time.
As well as degrading allelopathic chemicals, local soil
communities can alternatively enhance the allelopathic
potential of an exotic plant (Box 1). Phragmites australis
is a noxious invader in marshes in North America. Higher
levels of polymeric gallotannin were reported in the exotic
invasive P. australis plants compared to plants from native
non-invasive P. australis populations [25]. Higher pro-
duction and activity of tannase by native plants and soil
microbial communities in the non-native soils results in
the degradation of biologically inactive gallotannins to a
potent chemical, gallic acid, that might contribute to inva-
sion success of P. australis [25]. Experimental studies of
this potential mechanism and the proportional contri-
bution to Phragmites invasiveness have yet to be carried
out. These and other results in this area suggest that
degradation of novel chemicals by soil microbial commu-
nities, as well as adaptation to novel chemicals at the
species and community level might be involved in some
plant invasions.
Integration of mechanisms explaining invasiveness
The three pathways discussed above represent concep-
tually different types of soil microbial community involve-
ment in exotic plant invasions but they are to some extent
interlinked. For example, Blumenthal et al. [55] examined
the effects of a number of pathogens hosted by exotic
invasive plants in the USA, compared to effects in the
native ranges of the plants in Europe. Their results suggest
that plants from native resource-rich environments are
released more from pathogens in their non-native range
than plants from low resource habitats. This hypothesis
fits with the observation that many invasive exotic plants
are early succession weeds, since these can be most sensi-
tive to negative feedback effects from the soil community
[56]. Mid- and late-succession plant species, on the other
hand, have a more neutral to positive feedback interaction
with their soil communities [56]. Thus, release from (soil)
pathogens is more likely to enhance invasiveness of fast
growing plant species adapted to resource-rich environ-
ments than it is to enhance slow-growing plant species
from resource poor environments. Early succession weeds
are also more likely to disrupt mycorrhizal communities in
the invaded range, because the weeds are less mycorrhizal
dependent.
Exotic plants also have significant influence on catabolic
diversity of the soil microbial communities, which in turn
can influence nutrient cycling and ecosystem processes
[57]. The metabolic responses of soil microbial commu-
nities depend on the substrate produced by the exotic
plants and the microbial diversity in the soil [57]. It is
still uncertain whether or not invasive exotic plants
enhance litter decomposition and nutrient cycling [4].
One well-known example is that of invasion by Myrica
faya, an actinorhizal N-fixer, of young volcanic sites in
Hawai’i Volcanoes National Park. This has resulted in an
increase in the amount and mineralization of soil N, and
(Figure_1)TD$IG][ Review Trends in Ecology and Evolution Vol.25 No.9

Figure 1. Synthesis of pathways on the impact of soil communities on exotic plant invasion illustrating trade-offs between and among species or genotypes from low and
high resource areas. High resource species are strongly inhibited by enemies in their native range in comparison with low resource species [56], whereas species from low
resource areas have traded off growth against defense [64]. Species invading from high resource areas will have the disproportionate advantage of being released from
natural enemies [55,72]. Their low mycorrhizal dependence can lead to disruption of mycorrhizal communities [39,41,71]. As a speculation, accumulation of local pathogens
might be prominent in species from high resource areas, but there is a possibility that they will develop negative soil feedback with time since introduction [31]. Species
from low resource areas will be less competitive, provided that there are costs involved in the production of secondary plant compounds. This trait will be under negative
selection if it is less functional in the introduced range [53]. It is not known if novel chemistry is a trait of all exotic plant species, or just species from low(er) resource areas.
Novel chemistry could have negative consequences for nutrient mineralization, when it makes litter less decomposable.

has thus influenced N availability [58]. However, only few
invasive exotic plants fix aerial nitrogen. Effects of non-
nitrogen fixers on nutrient cycling can be highly variable
[59,60]. There has been relatively little work on the effects
of exotic plants on nutrient cycling and its influence on the
decomposition of allelochemicals in the soil [61,62].
Enemy release has both a short- and long-term
advantage, which lasts until native enemies develop on
the exotic plants [31]. The advantages of accumulating
local pathogens and producing novel chemistry, on the
other hand have an advantage that starts to become
operative only when the exotic plants have become estab-
lished; they first need to germinate, grow and produce
these biota and/or compounds [63]. Indirect evidence does
suggest that root exudates or leachates of Chromolaena
odorata encourage accumulation of native soil pathogens
in the plant’s invaded range in Western Ghats, India [34].
In principle, plants could have all three advantages of
enemy release, accumulation of local pathogens and the
production of novel chemicals, but there can also be trade-
offs between these traits (Figure 1), as has been argued for
growth versus defense in aboveground plant–enemy inter-
actions [64]. Moreover, these effects can be under selection,
so that they might vary over time during invasion history
[31,53] (Figure 1). Therefore, studies that aim to explain
the invasiveness of exotic plants should test a variety of
hypotheses and determine how these can combine (or not),
depending on the model species used for the study.
Concluding remarks
In conclusion, our understanding of the role of soil microbes
in the invasion success of exotics has progressed enor-
mously during the past decade. However, many questions
remain, largely because soil is often considered to be a
black box in many experimental studies. Examining how
plant–soil microbe feedbacks interact with ecological
disturbance, novel chemicals and soil fertility would shed
light on the role of soil communities in the functioning of
natural ecosystems before and after invasion. These stu-
dies would also stimulate debate about how belowground
interactions contribute to explanations of why relatively
few exotic plant species become so invasive [65]. There are
many methodological challenges in identifying the role of
particular soil microbes in plant invasion, including the
high diversity of microbes in soil, the difficulty of identify-
ing microbes to species level and the declining number of
microbial taxonomists [66]. Although it will be a daunting
task to establish the role of a particular soil fungus,

517
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bacterium or virus in the invasion success of exotic plants,
such efforts can provide a breakthrough in understanding
and predicting the course of plant invasions over time.
Acknowledgements
Inderjit is funded by the University of Delhi, Council of Scientific &
Industrial Research (CSIR) and the Department of Science & Technology
(DST). WvdP holds an NWO-ALW VICI-grant. We appreciate the
valuable constructive comments of three anonymous reviewers.
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