W. Mack Thompson
Colorado State University
Fort Collins, Colorado 80523
It is known that plants have defensive mechanisms that act directly against
herbivory and pathogen attack; however, recent studies have shown that a variety of
herbivore-damaged plants emit chemical signals that attract parasitoids and
predators to the herbivores. Plant utilization of "biological control" probably
evolved secondarily from chemical plant-defense responses, but may now represent an
important plant defense mechanism.а The phenomena of parasitoid/predator attraction
to herbivore-damaged plants has been studied for several plant-herbivore-
parasitoid/predator relationships.а These studies indicate that the parasitoid-
attracting signals released by plants are specific to both the plant-herbivore and
plant-parasitoid interactions.а Only certain herbivores cause the release of these
signals.а Artificial damage of plant parts does not elicit the same response as
herbivore feeding.а Additionally, the signals produced attract only certain
parasitoids.а The herbivore-induced emissions are also spatially and temporally
regulated.а The signals may only be emitted from the damaged area of the plant or
may be systemic in nature and emitted from other undamaged plant parts.а The signals
are also only produced during attack and decline slowly following attack.а For the
most part, the chemical identity of the parasitoid-attracting herbivore-induced
signals is unknown.а A recent study has implicated caterpillar b-glucosidase as an
elicitor of the plant response.а Numerous volatile compounds are stored in plants as
b-glucosides.а The glucosidase from caterpillar gut could cleave off the glucoside
and release the volatile compound.а The nature of these volatile compounds remains
unknown.а Avenues of future research include identification of parasitoid-attracting
herbivore-induce volatiles and studies that elucidate the coevolution patterns of
ааааааа Volatile infochemicals play an important role in tritrophic systems, systems
that include the host plant, herbivore, and parasitoid (or predator).а Parasitoids
must search for there hosts and many utilize volatiles from their host's habitat as
long-range cues to finding them (4, 5, 12, 14, 16).а These long-range signals appear
to come from the infested plants themselves.а This phenomena has been given several
names:а mutualism of plants and natural enemies (13), indirect defense (1), and as
stated above, tritrophic systems (16).а Each name carries its own connotations.а For
example, "indirect defense" may suggest that the plants specifically evolved the
ability to attract natural enemies of their herbivores, whereas "tritrophic systems"
simply indicates interactions among three trophic levels.а Regardless of the term
used, the interactions between plants and herbivore parasitoids can have a
significant impact on herbivore feeding and thus, such a characteristic could be
selected for in both the plants and parasitoids.а
ааааааа Tritrophic systems have a terminology based on context rather than chemical
nature (Figure1).а For example, a herbivore-induced infochemical from a plant that
is beneficial to the plant and parasitoid may be termed a synomone, but that same
chemical is a kairomone to the herbivore and parasitoid.а
Figure 1. Infochemical terminology (revised from (16)).
ааааааа A significant amount of research has been conducted on parasitoid-attracting
allelochemicals that are produced by herbivore-plant complexes (2-15).а This is a
very active area of research with the majority of studies conducted since 1990.
However, much of the work has been done haphazardly and only a few volatile
compounds have been isolated and verified as elicitors of this response (3, 4, 7,
13-15).а Several studies have involved isolation and identification of numerous
herbivore-induced volatiles from plants, but few studies have gone on to verify the
response to individual compounds and their combinations.а Much of the work has
focused on bioassays to determine preferences of the parasitoid for the plant
(undamaged, artificially damaged, and regurgitate treated), herbivore, or plant-
herbivore complex (1, 5, 6, 8-12).а The result is that at this time more is known
about the ecology of these interactions than the biochemistry (chemical ecology)
behind them, which makes it difficult to hypothesize the coevolutionary scheme that
has led to this phenomena.
ааааааа In this paper I will review what is known about the specificity of the
synomones and their regulation, and discuss several concepts that make this area of
research so interesting.
ааааааа Detectability vs. Reliability.а Parasitoids need signals that they can detect
over large distances and signals that reliably indicate the presence of a host (16).а
Kairomones from the host (herbivore) or its frass (11) are more reliable than
synomones from the plant (1).а Other signals include vibrataxis and sight (16).а
These signals are closely associated with the presence of a host, whereas synomones
from the plant may extend after the host has left the plant.а Additionally,
kairomones, vibrataxis, and sight tend to be more specific for the species of host
and even specific for host developmental stage.а Specificity is important to the
parasitoid so that it can avoid wasting time and energy seeking the wrong host
species or developmental stage.а These specific signals are used more in the micro-
habitat around the host because their detectability is limited (16).
ааааааа Herbivore-induced synomones are more detectable, but less reliable (specific)
(16).а Their increased detectability is mostly due to the large amount produced
compared to kairomones from the host itself (1).а Synomones are more distinguishable
between plant species than between different herbivores on the same plant, which is
expected since the plant produces the synomone (14).а Most differences between
herbivores feeding on the same species come from quantitative differences in the
synomone bouquet, however there can be qualitative differences such as the
production of different compounds (14).а Studies have shown that the ratios of
compounds in a herbivore-induced bouquet change depending upon the herbivore, but
exactly which combinations of chemicals and their ratios that participate in
attracting specific parasitoids is still unknown (1).а Quantity may simply be a
result of the amount of damage.а Large herbivores would cause more damage than
smaller ones (8).а Another important factor is the regurgitate of the herbivore.а
Differences in regurgitate from one species to another would most likely induce
qualitatively different synomones.
ааааааа Herbivore-induced synomones are important signals in long-range searching of
parasitoids for hosts mainly because of their detectability.а However, they can
contain enough information to be specific for certain hosts.а Other cues, such as
kairomones and sight, increase the specificity once the parasitoid has reached the
micro-habitat of the host.
ааааааа Spatial and temporal regulation of the synomone is important to the plant
(14).а There is most likely a cost associated with producing the synomone;
therefore, the plant would only want to produce the synomone when the parasitoid is
searching and when the herbivore is present.а Constitutive production would cost the
plant and the parasitoid because the parasitoid would waste time and energy on
plants with no hosts.
ааааааа Takabayashi et. al. (13) Divided herbivore-induced synomones into two classes:
1. Unconditional production which occurs when the interaction between the plant and
the parasitoid is unconditionally mutualistic.а This would be represented by a
general reaction by the plant to a herbivore at any time and the response of a
2. Conditional production which is divided into three types:
a) The plant should produce the synomone only when it is beneficial to the
parasitoid, i.e. only when infested with the host (herbivore) at the preferred
developmental stage for parasitism.
b) The plant should produce the synomone only when it is beneficial to the plant,
i.e. only when the plant is infested, during parasitoid searching times (to reduce
cost to the plant), and immediately following herbivory (to reduce impact of
c) The synomone should only be produced when it is beneficial to both the plant and
the parasitoid.а For example, in the C. kariyai-armyworm-cornа plant interaction, it
is conditionally mutualistic for the corn to attract the C. kariyai.а It is
beneficial for the corn to produce the synomone early when attacked by 1st-3rd
instar larvae because allowing the larvae to grow increases herbivory.а It is also
beneficial for the C. kariyai to respond to the early signal to beat other
parasitoids in finding unparasitized hosts.
ааааааа Spatial regulation of herbivore-induced synomones is also an important
consideration.а Many synomones are only released from the sight of herbivory, but it
may be in the plants best interest to release the synomones systemically, greatly
increasing the volume of the chemical bouquet (1).а This could lead to improved
attraction of parasitoids, but could also come at a cost to the plant.а
ааааааа Several studies have isolated volatiles from the head space of herbivore-
damaged plants (3, 4, 7, 13-15).а Some groups have only looked for compounds that
were produced after herbivory (4, 7, 13, 14), some bioassayed the mixture of
compounds (15), and a few have bioassayed individual components (3), however no
combinations of components have been studied.а Volatile components identified so far
include six carbon lipoxygenase-derived aldehydes, alcohols and their esters which
comprise the "green odors", terpenoids, and indole (1).а Some terpenoids, although
only a small percentage of the total head space, appear to elicit a response in
certain parasitoids.а Three terpenoids and methyl salicylate attracted females of
Phytoseiulus persimilis, but only the terpenoid linalool and methyl salicylate
attracted Amblyseius potentillae (3).а Emission of these chemicals was dependent on
herbivore damage and was not induced by mechanical damage alone.
ааааааа Is there a "universal type" of synomone?а Two homoterpenes, (E)-4,8-dimethyl-
1,3,7-nonatriene and 4,8,12-trimethyl-1-3(E),7(e),11-tridecatetraene, have been
observed to be herbivore-induced in many different tritrophic systems (1). The
enzymes needed to produce homoterpenes are wide spread in the plant kingdom, but so
is their production, such as in flowers and leaves of some plants, yet there
production is absent in some tritrophic systems (1).а Whether or not there is a
general class of compounds that fulfill the role of synomones remains to be
The fact that many volatiles are only produced in response to herbivory or to the
application of regurgitate to artificially damaged leaves indicates that something
associated with the herbivore elicits the response in the plant.а A recent study has
implicated b-glucosidase as a potential elicitor of herbivore-induce synomones (7).а
Plants often have terpenoids and similar compounds conjugated to glycosides. b-
glucosidases could cleave the glycosides and release these volatile compounds.а
Cabbage plants release volatiles that attract Cotesia glomerata parasitic wasps in
response to Pierie brassicae caterpillar feeding.а Mattiacci et. al. (7)
demonstrated that the regurgitant of the caterpillars contains b-glucosidase and
that almond b-glucosidase releases a similar blend of volatiles that is
indistinguishable to the parasitic wasps from the regurgitant elicited volatiles.а
The cabbage plants do contain their own b-glucosidase, but it is present in smaller
quantities and is not as active in producing the volatile compounds as the
caterpillar b-glucosidase.а Thus, it appears that b-glucosidase in the regurgitant
of P. brassicae is an elicitor of plant-parasitoid synomones.
Additional elicitors to b-glucosidase mostly likely exist since herbivores can
induce systemic release of synomones in plants.а It is generally thought that the
herbivore elicits the plant to produce the synomone systemically and that synomone
production not due to enzymes from the herbivore traveling throughout the plant (9).а
Spider mite infestation elicits a systemic response in Lima bean, yet spider mites
only contact the parenchymous cells and do not damage the phloem (1).а Therefore,
they couldn't transfer enzymes to the phloem indicating the plant must me producing
the synomone in response to herbivore attack.
A water-soluble endogenous elicitor has been extracted from the Lima bean-spider
mite system discussed above (2).а It produces parasitoid attracting volatiles when
fed through the petiole, but the compound is yet to be identified.а Thus, it appears
that the systemic response, at least in this system, is not due directly to
herbivore derived enzymes.а These results are one step closer to elucidating a
signal transduction system between the herbivore and the plant that produces a
synomone.а Two key factors that remain unknown are the elicitor from the herbivore
and the exact synomone(s) that are produced in response to that elicitor.
ааааааа Assaying for tritrophic responses is progressing rapidly, but identifying and
verifying the compounds that make up the synomones (parasitoid attracting volatiles)
is in need of further development.а Breakthroughs in herbivore elicitors and plant
elicitors are helping piece together the signal transduction pathways involved in
the herbivore-plant interaction.а Acquisition of the above information along with
what is already known about the specificity of the plant-parasitoid interactions
will provide more insight into the co-evolution of tritrophic systems.а Armed with
these tools, scientist may soon be able better the understand the role of indirect
defenses in plants and apply this knowledge to improve biological control of
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