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.

Introduction

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.

Signaling

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. 

а

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). 

ааа

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 

available.

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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