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Plant-modified trophic interactions
F. J. Frank van Veen
Centre for Ecology & Conservation
College of Life and Environmental Sciences
University of Exeter, Cornwall Campus
Penryn, Cornwall
TR10 9FE
UK
Correspondence: [email protected]; +441326255974
Abstract
Plants can modify the interactions between herbivorous insects and their natural enemies in various
ways. Chemical defences from the plants against herbivores may in fact harm the latter’s natural
enemies, thereby weakening the trophic interaction. On the other hand, volatile chemicals produced
by the plant in response to herbivory may attract natural enemies, thereby strengthening the
interaction. Recent research shows that effects of plants on insect interactions are not curious
phenomena confined to a few specialist species but rather that they are ubiquitous in terrestrial
ecosystems and often involve complex interactions among many species. The major challenge now is
to study how the commonly reported short-term effects of plants affect long term dynamics of
insect interactions in the context of complex natural communities.
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Introduction
The interactions between predators and their prey and parasitoids and their hosts have always been
central to the interests of ecologists: They are fundamental to our understanding of population
dynamics, community structure, and the (co-)evolution of many behavioural, morphological and
physiological traits. As well as being of such broad fundamental interest, the application of trophic
interactions in biological control means that they are of economic and food-security importance too.
Among insects, trophic interactions more often than not take place on the food plant of the
herbivorous prey/host. It is now clear that the plants are often far more than a passive arena on
which these interactions take place and they can have major effects on the strength of trophic
interactions among insects through two broad mechanisms (Figure 1): i) Plant defences that are
deflected by the herbivores unto their own enemies, reducing the strength of the trophic
interaction; ii) Plants producing volatile chemicals in response to herbivory which facilitate host/prey
detection by natural enemies, and thus increase the strength of the interaction.
These effects of plants on herbivore – natural enemy interactions can be considered in the
conceptual framework of ‘trait-mediated indirect effects’ [1,2]. In the context of the above two
mechanisms, this means that a plant indirectly affects the population growth rate of the natural
enemy by affecting a herbivore trait (toxicity), and/or indirectly affects herbivore population growth
rate by affecting a natural enemy trait (search efficiency). In either case the interaction between
herbivore and natural enemy is modified and trait-mediated indirect effects are therefore also
known as ‘interaction modifications’ [3]. These effects can have widespread consequences, affecting
population dynamics, the co-existence of species and even the trophic network structure of
ecological communities [4,5]. Given the dominance of plants and insects in biomass and biodiversity,
plant-modified trophic interactions could therefore play a key role in terrestrial ecosystems. In this
review I will focus on recent new evidence for these interaction modifications and I will investigate
the state of knowledge of, and evidence for, the expected widespread ecological effects.
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Herbivores use plant defences against their own enemies
One way for specialised herbivores to deal with plant chemical defences is to sequester the toxin.
This can have the added advantage (but not always [6]) of being able to redirect the toxins against
enemies [7]. Sometimes this may be an accidental by-product of the primary function of
sequestration but also more intricate mechanisms are at play. For example, Manduca sexta larvae
redirect nicotine from their host plants and exhale it to deter spiders [8●●].
Intuitively, turning plant defences against one’s own enemies may be expected to be the preserve of
some highly specialised herbivores and therefore to be an interesting curiosity of limited general
importance. However, plant defences may also affect the interaction between generalist herbivores
and their natural enemies, for example when the herbivore can survive a partially toxic diet which
results in it being a poorer host for its parasitoid [9●]. In such cases there may be no adaptive
advantage to the host of passing on the toxic effects if it still dies as a result of parasitism, but if it
leads to lower parasitoid recruitment then it may affect host-parasitoid population dynamics. For
other generalist herbivores, eating a mixed diet may lead to increased deterrence of predators [10].
The negative indirect effect of toxic plant species on the natural enemies of generalist herbivores
could lead to reduced top-down control of the herbivore population and therefore increased
herbivory on non-toxic plant species. It would be great if research in this field would start to include
explicit tests for such community-wide indirect effects.
Specialist natural enemies are more likely to evolve tolerances or defences against sequestered
toxins and therefore, on an ecological time-scale, plants are most likely to modify interactions
between herbivores and generalist enemies. Several studies do indeed report a negative effect on a
generalist predator but not on a specialist parasitoid [11] and a greater negative effect on the
development of a generalist parasitoid compared to a specialist [12]. Again, this has consequences
for the potential for wider effects on the community because it is the generalist enemies that can
couple the population dynamics of herbivore species that do not otherwise interact (“apparent
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competition”) and toxic plants could therefore weaken these indirect interactions. There are of
course always exceptions: Chinese mantids remove the gut of toxic monarch caterpillars but not of
non-toxic caterpillars, demonstrating that sometimes even generalist predators may evolve
mechanisms to overcome the sequestered defences [13].
The concentration of defensive chemicals also often varies among genotypes [14] and with plant age
which can cause complex effects on herbivore-natural enemy interactions. Junonia coenia feeding
on young Plantago plants have less access to defensive chemicals, making them more susceptible to
predation. Feeding on older leaves may provide better protection to predation but at a cost of
slower growth and compromised immune response to parasitoids [15●●]. Optimal diet choice for the
herbivore is therefore dependent on the (relative) population densities of predators and parasitoids,
which may themselves be coupled to the herbivore population dynamics and depend on herbivore
diet choice. Disentangling the population dynamic consequences of variation in plant defences is
therefore a serious challenge, but a very interesting one.
These recent examples reinforce that effects of direct plant defences on herbivore-natural enemy
interactions are widespread and may be accidental or sophisticated. They also demonstrate that,
due to the involvement of generalist herbivores and generalist natural enemies, complex community
interactions may be the result, the indirect dynamic effects of which remain to be explored [16,17].
Plants attract their enemies’ enemies
In a natural setting, with a high diversity of plants and insects, finding hosts or prey is not a trivial
matter for more or less specialised parasitoids and predators. While a random search maybe a good
strategy for generalists that can feed on most insect herbivores, the benefits of a targeted search
can be expected to increase with degree of specialisation. It has been known for many years that
natural enemies can use the smell of damaged plants, or ‘herbivory induced plant volatiles’ (HIPVs)
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to locate their hosts or prey [18]. From a plant perspective this is often referred to as indirect
defence [14], or plants crying for help [19], implying that the volatile emissions have evolved as a
means to reduce herbivory. An alternative explanation is that the volatiles have evolved for other
functions and that the natural enemy responses to them are a by-product. As yet, the evidence for
fitness benefits for the plants is limited [20,21●], although cases of increased egg parasitism due to
volatile emissions in response to herbivore ovipostion [22-25] must surely benefit the plant.
Regardless of the evolutionary background, HIPVs may play an important role in the population and
community ecology of insects with great apparent potential for application in biological control [26].
From laboratory to the field
Research on natural enemy responses to HIPVs is dominated by small-scale choice experiments in a
laboratory setting on a small number of model systems, which always raises questions about the
relevance in the real world. HIPVs are typically very short-lived chemicals so their effects may be
limited to short time spans and small spatial scales [27]. However, there are increasing numbers of
examples, ranging from grasses [28] to trees [23,29], that demonstrate the widespread nature and
ecological relevance of these effects in the field. An excellent example of joining up mechanistic
laboratory essays to large scale field experiments is a recent study on rice [28]. Gene silencing
techniques were used to create paired rice strains that differed only in their ability to produce
volatile chemicals. In laboratory choice essays, the inducible S-linalool was shown to attract
parasitoids and predators but to repel the major pest herbivore Nilaparvata lugens. This was
followed up with a large scale field experiment in which the invertebrate communities on replicate
plots of transgenic plants were compared with those on the non-transgenic counterparts and the
results from the laboratory essays did indeed translate to the field. The plants that did express Slinalool grew larger in the presence of insects (field), but not in their absence (laboratory), indicating
that the effects on the insects are of real significance to the plant growth at the population level.
Ecological complexity
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The dominant subjects of research on natural enemy responses to HIPVs have been parasitoid wasps
[21]. Some of this may be historical but there are good biological reasons too. Parasitoids are
generally more specialised than predators and because of the often specific nature of volatiles
produced in response to different herbivores one would expect that specialist natural enemies will
be more in tune with HIPVs than generalists. However, this is not always the case among parasitoids
[30] and generalist may be better at learning to make associations [31]. HIPVs rarely affect only a
single species. For example, volatiles produced by tomato plants in response to aphid feeding attract
generalist predators as well as specialist parasitoids of aphids as well as those of other herbivores,
which may themselves be repelled [32]. Braasch et al [33] tested for effects of three HIPVs on 119
arthropod taxa in the field and found responses in four to sixteen species, dependent on the crop
species. Although these may be regarded relatively small proportions, the taxa that responded
included herbivores, parasitoids and predators which demonstrates the potentially complex changes
in interactions even in simplified agricultural systems. A major challenge to the field therefore, is to
extend the knowledge from simple one-species-per-trophic-level systems to the ecological reality of
interactions in a community context [19,20,34]. Inevitably, such studies will have to take on a multigenerational approach as many of the direct and indirect effects are on vital rates that affect
population growth rates and therefore the coupling of the dynamics of multiple species.
One of the few areas where the community dynamic effects of HIPVs have been studied is when
feeding by multiple herbivore species affects the volatile blends emitted by the plant and thereby
alters the interaction between each herbivore and its natural enemy [35,36]. The presence of
multiple herbivore species may have a negative effect on the ability of parasitoids to locate suitable
host species, either due to non-specificity of signals (homing in on the ‘wrong’ host) or due to
chemical ‘noise’ (can’t smell the wood for the trees) [37]. The multi-generational effects of this kind
of interference of parasitoid searching efficiency have been studied both theoretically and
experimentally and have been shown to be a strong mechanism for stabilising host-parasitoid
dynamics of species that are highly extinction-prone when isolated from the community [38-40].
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An alternative perspective of essentially the same effect is that invasive herbivores may affect the
infochemical network and reduce the search efficiency of native parasitoids for their native hosts
[41]. It is interesting to note here that the same effect (interference) can be regarded as a good thing
(population persistence) or a bad thing (reduced impact of natural enemy of herbivore), depending
on the time scales of the perspectives: multi-generational population dynamics versus single
generation effects.
As well as attracting the natural enemies of the herbivores, HIPVs may also interact with other
insects that affect the plant and the herbivore-natural enemy interaction. Key among these are
enemies at the next trophic level, e.g hyperparasitoids or parastoids of predators [20,42,43].
Interestingly, volatiles from hyperparasitoids have been shown to repel primary parasitoids [44] and
even lead to higher reproductive output of aphids [45]. There exists therefore the potential for
complex negative feedback from HIPVs and the multi-generational effects of these are difficult to
predict without dedicated modelling and experimentation – work that has yet to be done.
Another major insect group that respond to plant volatiles are pollinators. HIPVs produced by wild
tomatoes repel pollinators to the extent that herbivory leads to a reduction in seed-set due to pollen
limitation rather than direct herbivory effects on plant resources [46]. Plant volatiles can also play an
important role in attracting pollinators [47] but enhancing these volatiles can have the undesirable
side effect of attracting florivorous beetles, leading to a net reduction in plant reproduction [48].
These examples illustrate the potential ecological complexity that can hamper the application of
induced volatiles in real crop systems: positive effects on crop production by affecting the intended
target insects (e.g. parasitoids) may be overshadowed by unexpected negative effects via other
species.
Conclusions and future directions
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It is really quite striking how ubiquitous plant-modified trophic interactions are. Rather than being
the curious phenomenon I remember hearing about when I was an undergraduate student, they
appear to be the norm in what are, after all, the dominant components of terrestrial ecosystems. It
is encouraging to see the increasing linkage between small-scale laboratory experiments and large
scale field studies which allow for detailed mechanistic knowledge to be tested for ecological
relevance and for this knowledge to be applied to biological control of crop pests. There are also an
increasing number of studies that go beyond one-species-per-trophic-level systems and that
explicitly test for community context, because, even in agricultural settings, the norm is of multiple
interacting species [49●●].
However, one thing that struck me during my literature searches for this paper was that the vast
majority of experiments only study short term effects. The response variables are mostly parasitoid
choice in olfactometers, or parasitism rates within single host cohorts but I could not find a single
recent example in which multi-generational effects were studied. Whether biological control or
fundamental ecology are our main motivators, the effects on long term dynamics should surely be
top of the agenda. In addition, important questions of spatial scale [26] and eco-evolutionary
dynamics in complex community and landscape settings remain [50]. While advances in
understanding the genomic and other mechanistic aspects of the plant - insect interactions are
exciting and fascinating, and open the way to practical applications [26], the next major challenge
must be to work towards understanding their role in multi-generational dynamics in the context of
complex natural communities.
Acknowledgements
The author’s research time on indirect interactions is funded by the UK Natural Environment
Research Council, grant reference NE/K005650/1.
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Figure caption
Figure 1. Two ways in which plants can modify the strength of trophic interactions between
herbivores and their enemies: The interaction may be weakened when the plant’s chemical antiherbivore defences harm the natural enemy when they feed on the herbivore; The interaction may
be strengthened when volatile chemicals emitted by the plant attract the natural enemy, allowing it
to discover prey at a higher rate.
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