The Role of Plants in Attracting Predators and Parasitoids to Control Herbivore Feeding

Julie McIntyre
Colorado State University
Fort Collins, Colorado 80523
Plants may take an active part in defending themselves from severe herbivore damage 
by attracting carnivorous arthropods.а Studies have shown that plants damaged by 
herbivore feeding produce chemical cues which signal natural enemies on where to 
find prey.а Volatile chemical compounds emitted from plant tissue most likely 
originated to repel the attacking pest, but also serve a secondary function, 
attractants to parasitoids and predators in search of prey.а Plant phytochemical 
responses are most likely induced by the interaction of substances from the 
herbivore with plant tissue. These volatiles, primarily determined to be terpenoids, 
differ from those emitted in response to mechanical damage.а Several studies have 
been conducted on these compounds, termed exogenous herbivore elicitors of plant 
responses, including work with spider mites and different lepodopterous 
caterpillars. These chemicals are specific volatiles which affect predator foraging 
behavior in a range of behavioral responses.а The ability of the natural enemy to 
recognize chemical cues and identify its source of origin determines its 
effectiveness as a predator. Qualitative differences occur between the odors emitted 
by different plant species which the predator can distinguish from each other as 
well as from background odors.а In addition, predators show some ability to learn 
and distinguish between odors not only from different herbivore species but also 
between different plant species.а Studies have examined these interactions in a 
variety of systems.а Lima bean plants infested with the mite Tetranychus urticae 
produce terpenoids and methyl salicylate which attract the predator mite 
Phytoseiulus persimilis.а Substances found in caterpillar regurgitant are necessary 
for the plant to begin manufacturing and releasing indole, terpenes and 
sesquiterpenes which attracts the parasitoid Cotesia marginiventris..а Investigation 
of exogenous elicitors continues in order to enhance biological control capabilities 
by manipulating attraction mechanisms of predators and parasitoids.
аааа Plant defense against herbivores has traditionally been studied in a bitrophic 
context, that is to say in a predator-prey or predator-plant context.а But with 
further research, it has become more evident that the plant can directly influence 
predator-prey populations on itself. Studies indicate that a plant signals for the 
influx of natural enemies to eliminate herbivores from feeding on it. When the plant 
is considered in this intercommunication, then defenses can be studied in a 
tritrophic context: plant-herbivore-carnivorous arthropod (Dicke 1990).а This 
acknowledges that there is a signaling interaction between the plant and the insect.а 
A plant▓s means of defense has traditionally been viewed and studied as a ⌠direct 
defense■ (Dicke and Sabelis 1988).а This comprises a plants production of toxic and 
repellent chemical compounds to directly dissuade insects from feeding on tissuesа 
Within a tritrophic framework, plant defense can be viewed as ⌠indirect defense■ 
(Dicke and Savelis 1988; Dicke 1993); the plant may be involved in the control of 
carnivorous arthropods by attracting their natural enemies.
аааа There remains some question as to what exactly the evolutionary development of 
these chemical signals has been.а Did the plant evolve so as to release volatiles in 
order to attract the natural enemies of the pest?а Or are the insect carnivores 
eavesdropping on a chemical plant defense system aimed at the attacking pest.а It is 
thought that the plant does undergo physiological changes which increase the level 
of toxins expressed in the tissues, thus making the plant unpalatable for further 
herbivore damage.а As seen in corn and cotton plants, herbivory over time causes the 
plants to become less palatable to the feeding larvae, corresponding to the increase 
in production of herbivore induced volatiles (Stowe et al, 1995).
аааа Studies have shown that foraging behavior of carnivorous arthropods relies on a 
variety of stimuli to locate hosts (Geervliet 1994;Lewis 1990; McCall et al 
1993;Dicke 1994)а Chemical cues play a major role in information gathering; they may 
come from the herbivore, from the plant, or from the interaction of the herbivore 
and the plant.а Whichever it may be, it is essential that the carnivore be able to 
detect these chemicals cues and identify them.а The most reliable cues come from 
chemicals emitted from the herbivore itself.а These most directly and clearly inform 
a carnivore of a suitable prey▓s presence.а But these are difficult to detect long 
distances away (Geervliet 1994).а Plant derived cues are thought to be more 
detectable, even at longer distances (Steinberg 1993).а So if a carnivore is to be 
successful at foraging, it needs to maximize its ability to recognize foraging cues 
so it can survive and ultimately reproduce.а The process of natural selection then 
has chosen for those carnivores that can readily detect reliable foraging cues.а 
Fortunately for the plant, the most reliable long-range foraging cures for 
predators/parasitoids are the herbivore induced plant volatiles.а This form of 
intercommunication allows for the continued survival of each species≈the plant rids 
itself of damaging pests and the insect carnivore finds food.
аааа In order for a plant to effectively defend itself against damage done by 
herbivore infestations, it has to formulate chemical cues that can be heard, 
understood and acted upon by the natural enemy of the herbivore.а These three 
criteria are the basis for plant chemical defense by attraction of predators and 
parasitoids (Turlings 1995) and have been witnessed in numerous plant-insect 
interactions.а The plant summons for help by producing volatiles that a predator can 
separate and distinguish from the bouquet of background odors that exist in an 
insects world at all timesа Signaling has to be specific enough to target an insect 
carnivore as well as foretell of available and suitable prey.а This communication 
involves specialized cues that can vary depending on the plant-insect combination.а 
It also entails that these signals be emitted at a time when the insect carnivore is 
actively seeking prey. 
Clarity of signal
ааааааа Chemical signaling by the plant is going to influence how successful a 
parasitoid is in locating and recognizing potential hosts, and consequently how 
effective a plant is in defending itself.а Therefore, it is necessary for these 
signals to be identifiable and distinct enough for the parasitoid to separate from 
other odors.а Parasitoids respond to odors directly linked to the host, reliably 
indicating their presence, identity, and suitability (Steinberg 1993).а The 
parasitoid may rely on chemical cues emitted by the host itself (eavesdropping on 
pheromone signals from the host), on the products the host produces (larvae or 
feces), or on the damaged plant on which the host is feeding (Lewis 1990).а Of these 
three factors, the volatiles emitted from the damaged plant are the most attractive 
to the parasitoid (Turlings 1990; Geervliet 1994).а As an example, the female 
parasitoid, Cotesia marginiventris, was not attracted to odors from beet armyworm 
larvae, Spodoptera exigua, themselves, but to the volatiles emitted from the damaged 
corn plant upon which they fed (Turlings 1995; Turlings 1990).а Overtime, fed on 
corn plants produced chemical compounds, terpenoids and indole, which attracts the 
parasitoid.а The length of time the plant is fed on determines the type of chemicals 
produced by the plant, and thus how attractive it may be to Cotesia.а Chemicals 
emitted within one hour of feeding tended to be lipoxygenase-derived volatiles 
(green leaf volatiles) fatty acid derivatives such as C6 aldehydes andа alcohols 
(Dicke 1994) while chemicals emitted after 6 hours of feeding were terpenoids 
(Turlings 1995).а The odor of a plant can be made up of hundreds of chemicals which 
can be either very unique to a plant, or common among them (Ramachandran 1991).а For 
the parasitoid, green leaf volatiles are harder to separate from background odors.а 
These odors are also more difficult to trace the origin of emittance, and generally 
not too attractive to parasitoids.а Interestingly, artificially damaged tissues 
release green leaf volatiles, not terpenoids, thus avoiding sending out false alarms 
to parasitoids.а Artificially damaged plants can be induced to emit volatiles if 
caterpillar regurgitate is added to the wounded site (Turlings 1993).а A substance 
in the spit interacts with plant tissue to cause the wounded plant to begin 
manufacturing and broadcasting terpenoids.
аааа Other means the plant utilizes to ensures its distress signal is clear to 
parasitoids is to release the volatiles systemically.а All leaves, whether suffering 
from direct feeding damage or not emit parasitoid-attracting terpenoidsа The plant, 
in effect, makes itself stand out like a beacon in a wealth of odors so that it can 
be found by the parasitoid.а This systemic effect can be demonstrated by placing cut 
seedlings into diluted caterpillar regurgitate; after a number of hours there is a 
significant increase in terpenoid emissions from all the leaves of the seedling.а C. 
marginiventrisа are attracted to these terpenoids and will have little trouble 
locating the source of origin (Turlings 1995). 
аааааA plant can also ensure the strength and clarity of a signal by manipulating 
the amount of volatile released.а One herbivore damaged corn plant will emit several 
micrograms of compounds per hour.а A considerable amount when compared to pheromone 
communication which only produces a few nanograms per hour (Turlings 1995).а 
аааа Studies on spider mite and predatory mite interactions have confirmed the 
emission of herbivore induced terpenoids to prevent detrimental infestations by 
effectively attracting predators to control populations (Dicke and Sabelis 1988).а 
Lima bean plants were found to produce a volatile which was attractive to predatory 
phytoseiid mites, Phytoseiulus persimilis, when the plant was under attack by the 
two-spotted spider mite, Tetranychus urticae.а Similarities between the corn and 
lima bean plants are prevalent, even though the systems appear to be quite 
different: monocot vs. dicot host plants, arachnids vs. insect herbivores, and an 
arachnid predator vs. a parasitoid.а However, spider mite infested lima bean plants 
have been actively defending themselves against attack in similar ways.а Lima bean 
plants also produce terpenoids as well as the phenolic methyl salicylate.а The 
strength of the signal is heightened by releasing them systemically; volatiles are 
transported out of infested leaves into uninfested parts of the plant (Dicke et al 
1993).а These volatiles are not emitted with mechanical (artificial) damage either, 
indicating the herbivore-plant interaction.а 
аааа The clarity of the signal emitted by the lima bean plants was demonstrated by 
placing petioles from infested leaves into water, removing them and then replacing 
them with the petioles of uninfested control leaves.а In an olfactometer 83% of the 
predatory mites preferred those leaves which had been placed in previously infested 
leaf water over control leaves which had never been infested.а Overall, 82% of the 
mites preferred infested leaves over uninfested control leaves (Dicke et al 1993).а 
Clearly, the signal the plant is emitting is not to be mistaken by P. persimilis and 
it utilizes these chemicals to search for prey.а This indicates that there is a 
water soluble systemic volatile produced by the plant which was transferred through 
the water into leaves that had never been directly infested with mites (Dicke et al 
1993). In addition, mites given a choice between water in which the petioles of 
infested and uninfested leaves had been placed showed no preference, indicating the 
attractants are not contained in the water itself. 
аааа Plants seem to be successful in ensuring that chemical cues are discernible to 
predators and parasitoids.а Terpenoids were probably originally produced as a direct 
defense against the herbivores themselves, but served a secondary function of 
signaling and attracting carnivorous arthropods (Turlings 1990).а In turn, these 
volatiles have been exploited by predators and parasitoids to locate prey and hosts.а 
Over time, the selection process and adaptation has refined the signaling 
capabilities of these chemicals in plants, which has resulted in the present day 
form of chemical communication between plant and insect.а Because terpenoids are 
produced only upon herbivore damage, not from artificial damage,а the plant signals 
to the parasitoid that hosts are present.а Whereas with mechanical damage only, 
green leaf volatiles are not discernible from background odors and provide no 
communication for the parasitoid.а As these cues are emitted systemically and 
expressed throughout the entire plant, the strength of the chemical signal is 
intensified.а Add to this a large quantity of the volatile produced, and the 
reliability of the signal is ensured (Turlings 1995).а These chemical cues need now 
only to be interpreted by C. marginiventris or by P. persimilis; they need to 
indicate that there is suitable hosts or prey for them.
Specificity of Signal
аааа It has been determined that insect carnivores can differentiate between 
chemical cues emitted by uninfested plants, mechanically damaged plants, and plants 
infested by a specific herbivore species (Steinberg 1993).а It is thought that 
predators and parasitoids are led to their prey by general stimuli and then learn 
more specific stimuli to assist them in narrowing down the options (Geervliet 1994).а 
Herbivore induced volatiles provide these specific cues for the carnivorous 
arthropods to follow. However, this evolves into quite the formidable task when the 
hosts may feed on a number of different plant species.а In agricultural settings, 
this may not present that great of challenge as cropping tends to consist of 
monocultures.а Still, the carnivore has developed the ability to differentiate 
chemical signals in a sea of possibilities.а This ability could be attributed to 
different concentrations of chemical cues which cause different behavioral actions 
in the hunter.а This preferential searching may also be influenced by the plant 
species or the quality of volatile emitted which is determined by the growth stage 
and cultural conditions of the plant, the part of the plant is being attacked, and 
the species of herbivore is doing the attacking.а (Geervliet 1994; McCall 1993).а 
Specialist parasitoids such as Microplitis croceipes whose hosts feed on a range of 
different plant species have shown the ability to differentiate between different 
types of damage on different plant species.а Cotton, cowpea and soybean each produce 
a particular blend of chemicals when fed on by the same herbivore, corn ear earworm 
caterpillars.а Volatiles may also differ depending on which part of the plant is 
being damaged: flower volatiles differ from chemicals of damaged leaves.а C. 
marginiventris, which as a generalist feeds on different species of moth larvae for 
example, has to be able to recognize two different volatiles produced from the same 
plant, one emitted from the fall armyworm and one emitted from the beet armyworm 
(Stowe et al 1995).а Predatory mites have also been shown to discriminate between 
different blends of signals emitted from varying spider mite species and plant 
combinations (Dicke 1993).
аааа Because of the large variability in chemical cues, it serves the insect 
carnivore well to be able to learn different volatile mixtures.а Studies with M. 
croceipes revealed that the more experience wasps gained the better able they were 
to discriminate between odors.а Wasps were able to learn odors and associate them 
with specific populations of hosts.а With one experience, wasps were unable to 
differentiate between known and unknown odors and would fly to a known odor just as 
often as to an unknown odor.а But, after three experiences, the wasps would choose 
the known odor.а They were able to discriminate between the odors and chose the odor 
where they had previously been successful in finding hosts.а However, some research 
has shown that wasps have difficulty in determining host damaged plants form non-
host damaged plants (McCall 1993).а Specialist parasitoids have been shown to learn 
different odors emitted from different caterpillars feeding on the same plant 
variety.а C. marginiventris was able to distinguish between volatiles emitted from 
S. exigua and S. frugiperda feeding on corn (Turlings 1995).
Signaling the Forager
аааа As has been demonstrated predators rely on a large amount of chemical 
information in order to be effective at foraging.а Larvae had evolved so at to be 
quite inconspicuous and difficult for insect predators or parasitoids to detect; 
they are difficult to detect with visual stimuli and they do not emit chemical 
signals.а However, the larvae need to feed and it is at this point where they 
inadvertently give themselves away.а Exploitation of insect herbivore-induced 
chemicals cues from feeding damage provide the basis of information for predators 
and parasitoids.а In this case, it is essential that the plant responds with its 
distress call at a time when the predator or parasitoid is available to receive the 
signal.а Recent studies indicate that there may be some variability in the rate of 
emission of volatiles over the course of the day (Stowe et al 1995).а Peak emissions 
were found to occur during the photophase which also is the time of carnivore 
foraging.а Additional studies have shown fluctuating emission of volatiles during 
different growth stages of the plant, as well as with different parts of the plant.
аааа Corn seedlings respond to herbivore damage by a delayed release of terpenes and 
sesquiterpenes.а Initially upon feeding the volatiles cannot be separated from green 
leaf volatiles which have no attraction to an insect carnivore.а Terpenoidsа are 
probably stored in glands in the leaves and are ruptured upon feeding.а Release of 
these compounds stops as damage stops, i.e. when the caterpillar no longer chews on 
them.а However if the caterpillar is not removed the emission slowly wanes over time 
as quantities lessen and caterpillars feed less.а The release of these terpenoids 
begins only after several hours of being fed on.а Terpenoid emissions seem to be 
strongest during daytime hours and when caterpillar regurgitate was placed on 
damaged tissue, terpenoid emission was detectable three days later.
аааа Plants do respond readily to damage and with enough alacrity to signal for 
predators or parasitoids.а In addition to releasing volatiles systemically, the 
volatiles are released during the day when carnivores tend to forage.а There is 
still some question as to whetherа these emissions are released at that time because 
that plant has adapted to predators searching hours or if the predators search 
during the photoperiod because that is when the majority of chemical cues are 
Prospects for Application
аааа With the knowledge of how these communication systems operate, they can be 
manipulated by man to maximize performance of biological control measures in 
agriculture.а If the mechanisms of what attracts and retains a predator or 
parasitoid to a field are understood, they can be developed and enhanced to optimize 
control possibilities (Lewis 1990).а The insect carnivore can be retained in the 
field after mass release and the efficiency of search and attack maximized.а 
Exogenous elicitors may be developed synthetically, applied to a crop and utilized 
to increase the time of searching by the natural enemies.а Plant breeding may 
produce crops that are able to produce more volatiles making them even more 
effective in attracting natural enemies (Stowe 1995).а The application possibilities 
from herbivore induced volatiles research will prove to be as intriguing as the 
research itself.
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