Parasitoid Host Selection: Host and Host Food-Plant Cues

Walter Roachell
Colorado State University
Fort Collins, Colorado 80523
Successful parasitism by parasitoids of herbivorous insect hosts is preceded by 
several phases of host searching that lead females into the close vicinity of their 
potential host(13).а In each of these phases, the female often utilizes chemical 
stimuli to guide her in the search forа a suitable host.а Chemical stimuli emitted 
by members of the different trophic levels in the parasitoid's environment, such as 
the herbivorous host or the host's foodplant, are often used in the host-searching 
process(5).а Host derived stimuli are the most reliable indicators of the presence 
of hosts, but they may be hard to detect at long distances, whereas plant-derived 
stimuli are assumed to be more detectable(1).а 
The role of stimuli from different trophic levels in various phases of the host-
searching process, is hypothesized to be determined by the parasitoid's degree of 
specialization(1).а Specialists have been shown to exhibit behavioral responses to 
host-de rived cues, such as herbivore products and the herbivore itself, or to 
specific herbivore induced synomones.а For generalist, such fixed responses to 
specific stimuli do not seem to be functional or may be impossible due to more 
physiological constraints co mpared to specialist.а It has been hypothesized that 
the generalist is guided to their host by more general stimuli at first and 
subsequently learn to respond to more specific stimuli(11).а 
Due to the impressive variety of specialized lifestyles found in insect parasitoids, 
generalizations about their foraging behavior may be considered difficult to make.а 
Certain characteristics of the host's ecology can be important in the evolution ofа 
specific foraging mechanisms in parasitoids and in determining the usefulness of 
different sensory modalities in this foraging(12).а Host-derived cues provide the 
parasitoid with very specific information as to the identity of the prospective 
host, but usua lly these cues are in such low levels that they are hard to detect.а 
On the other hand, cues from the host's food plant have a much higher degree of 
detectability, but generally have a low reliability.а The purpose of this review 
article is to examine the foraging mechanisms of parasitoids, and determine how the 
reliability-detectability problem is solved.а <:s>
Many natural enemies are known to discriminate between volatile chemicals emitted by 
uninfested and herbivore-infested plants.а Chemical stimuli emanating from the 
plant-host complex can originate from the herbivore, the plant, or from interactions 
bet ween the herbivore and the plant.а In spite of the lifestyle diversities, insect 
parasitoids have certain aspects of foraging in common.а Long distance location by 
parasitoids seems to be essentially guided by information from the food of the host, 
whileа at shorter distances information from the host itself becomes increasingly 
important.а Parasitoids encounter a great variety of stimuli that they may use in 
host location.а The appropriateness and usability of this information depends on two 
factors:а 1) its reliability in indicating host presence, accessibility and 
suitability and 2) the degree to which stimuli can be detected(12).
Stimuli derived directly from the host are generally the most reliable source of 
information because they can inform the parasitoid of the presence, identity, 
availability and suitability of the host.а Although this type of stimuli has a high 
reliability, it is often limited by low detectability.а Low detectability of host 
derived information has two inherent constraints that limit its use as stimuli for 
host location.а In terms of mass, hosts are small components of a complex 
environment and if they produce any information at all, it will be small in amount.а 
Secondly, there should be constant selection on the hosts for inconspicuousness as a 
way to avoid parasitization and predation(12).а 
As stated above, one of the constraints of host derived cues is the relative small 
amounts of volatiles produced by the host.а Host derived cues are difficult to 
detect at long distances and thus become more important the closer the parasitoid 
gets to the host.а There are however several types of host cues that are used by 
some parasitiods to locate hosts from long distances.а While communicating 
interaspecifically through pheromones, herbivores are often much more conspicuous to 
their natural enemies th at exploit these pheromones as kairomones in long distance 
herbivore location(14).а A well known example is that of predators and parasitoids 
of bark beetles that respond to volatile aggregation pheromones of their victims.а 
Similarly, parasitoids exploit the sex pheromones of their hosts as kairomones(2).ааа 
Various pieces of direct and indirect evidence indicate that within a habitatа 
Trichogramma spp. are able to distinguish between host-infested and uninfested 
areas.а In this phase, foraging behavior seems to be mediated by odors originating 
from adult female host insects(11).а Studies have been done that deal with the means 
byа which Trichogramma detect host communities within a habitat.а This research has 
provided evidence that suggests that the sex pheromone of the host may play a 
significant role in this respect.а 
The eggs of the cotton bullworm, Heliothis zea, were found to be heavily parasitized 
by naturally occurringа Trichogramma spp. in cotton plots treated with synthetic sex 
pheromone of H. zea than in control plots(2).а These findings aroused the interest 
of several researchers as to the behavioral mechanism underlying the observed 
effect.а Increased parasitization in treated plots could be due to attraction of 
parasitoids from a d istance.а Noldus & van Lenteren studied this problem in a 
comparable host-parasitoid system:а the cabbage armyworm,а Mamestra brassicae and T. 
The experiment consisted of a bioassay using calling virgin moths as the order 
source.а The basic set-up consisted of a four-armed airflow olfactometer.а Three of 
the virgin moths were placed in a glass cylinder, which was then connected to one 
arm ofа the olfactometer.а A second glass cylinder containing 3-5 male moths was 
attached to the exhaust air stream, and their behavior was used as a check for the 
actual presence of sex pheromone in the air stream.а A parasitoid was released into 
the olfactometer chamber only after calling activity of at least two of the male 
moths had been observed. The parasitoid was observed for 10 minutes(4).а 
During the 10 minute observations, the parasitoids made a significantly higher 
average number of visits to the flow field containing the odor of the moths than to 
the opposite control field.а The insects stayed significantly longer in the flow 
field co ntaining the odor of the calling moths compared to the control fields(4).а 
These results demonstrate that T. pretiosum can show a behavioral response to the 
odor emitted by callingа H. zea moths.а The fact that a reaction of the wasps was 
elicited only by female moths during calling activity and concurrent with male moth 
responses, strongly suggests that the parasitoids were indeed responding to the sex 
pheromone of the moth.а The reaction of T. pretiosum to its host's sex pheromone may 
be illustrative of many species of egg parasitoids(4).ааа 
The research seems to confirm that the sex pheromone of H. Zea serves as a kairomone 
for T. pretiosum.а Noldus et al surmises that it indeed seems adaptive for an egg 
parasitoid to use host sex pheromone as an indicator for the probable presence of 
host eggs, because as far as known no other long distance c ues more directly 
connected to the eggs themselves are available(4).аа 
Apart from the use of host pheromones, herbivore odors are difficult to detect at 
long distances.а As expected, herbivore derived cues become more important the 
closer the foraging parasitoid comes to their host.
Stimuli from the food of the host or prey are usually more readily available, 
because of the food's relatively large biomass, but are less reliable predictors of 
host or prey presence and suitability. The amount of herbivory on the plant strong 
ly affects the usefulness of the volatile cues from the plant.а If the infestation 
is very high, information from the plant is very reliable, and can even replace the 
more difficult-to-detect host information(12).а 
Plants show some astonishing adaptations that promote the presence of predators and 
parasitoids.а A good example of this is the relationship between acacias and ants.а 
Specialized structures on the acacia provide the ants with food and shelter.а The an 
ts seem offer the plants protection against herbivory.а In light of the astonishing 
adaptations plants exhibit, it should not be surprising that some have proposed that 
plants may actively guide the predators and parasitoids to the herbivore(6).а Recent 
stu dies have revealed that plants that are under attack by herbivores initiate the 
release of chemical "signals" that parasitoids use to locate their victims.а 
Herbivore-induced plant chemical responses are usually considered direct defenses 
against the herbivorous attackers.а Herbivore-injured plants release relatively 
large amounts of volatiles that are attractive to parasitoids.а Since the plant and 
the pa rasitoid both benefit from this interaction it has been suggested that the 
plant responses serve to recruit the parasitoids.а Turlings and Tumlinson argue that 
induced production of plant chemicals evolved first as a direct defense against 
herbivores, and that the attractive function evolved secondarily(8).а Three aspects 
ofа plant signal seem most relevant to the ongoing discussion on whether or not 
herbivore damaged plants actively lure natural enemies.а (a) The signal should be 
clear enough to the insectsа so that it can be perceived and distinguished from 
background noise.а (b) The signal has to be specific enough to reliably indicate the 
presence of a suitable host or prey.а (c) The signal will have to be emitted during 
the period of time that the natural enemies forage(6).
Turlings and Tumlinson studied the host searching behavior of the parasitoidа 
Cotesia marginiventris, and discovered that plants emit a strong odor when under 
attack by caterpillars.а Rather than responding to odor cues coming directly from 
their hosts, females ofа C. marginiventris are strongly attracted to volatiles 
emitted by the caterpillar damaged plants(9).а Research focusing on the 
identification of the emitted chemicals revealed a clear difference between corn 
seedlings that were under recent herbivoreа attack and seedling that had been fed on 
for more that six hoursа 
Fresh feeding damage results in a significant release of (Z)-3-hexenal, (E)-2-
hexenal, (Z)-2-hexenol, (E)-2-hexenol and (Z)-3-hexenyl acetate.а These volatiles, 
also known as "green leaf volatiles" are the only compounds detected at this stage.а 
Afterа several hours, however, emission of large amounts of terpenoids were 
observed. (figure 1)ааа 
It was found that this emission of specific chemicals could not be induced by 
mechanical damage alone.а Plants that had been fed upon by caterpillars for 2 hours 
released far more of these terpenoids on the following day than plants that had been 
dama ged with razor blades during the same 2 hours.а When caterpillar regurgitate 
was applied to sites that had been freshly damaged with a razor blade, the plants 
released terpenoids in amounts equal to those released by caterpillar damaged 
Signals from herbivore damaged plants are further enhanced by the fact that the 
chemical emissions are not limited to the damaged sites.а For corn seedlings, all of 
the induced compounds are released throughout injured plants.а Unharmed leaves of 
dama ged plants show an increase in the release of terpenoids(8).а The chemicals 
emitted by the plants upon herbivory should be easily detected by insects and thus 
could serve as very clear signals to parasitoids and predators.а The amount of 
volatiles producedа per hour by the plant is much greater than the amounts normally 
seen in insect pheromone communication.а Only a few nanograms of sex pheromone per 
hour can be detected a compared to several micrograms of a particular substance 
emitted by one corn seedling(8).а 
Turlings and his group conclude that the chemicals emitted by the plants in response 
to herbivory are easy to detect by insects and are clearly distinguishable from the 
extremely low levels of odors emitted by unharmed plants.а Moreover, the blend of 
induced terpenoids emitted by herbivore damaged plants is quite different from the 
odors emitted by unharmed or mechanically damaged plants.а Unlike the "green leaf 
volatiles" and constitutive terpenoids that may be released by mechanical damage, 
the inducedа substances represent a signal that is dependably associated with the 
presence of herbivores.а The signal is enhanced by the systematic nature of the 
plant response and makes the whole plant stand out as an odorous beacon that should 
be easily distinguishable from the surrounding plants.а In short, herbivore injured 
plants provide foraging natural enemies with a very clear odorous signal that 
indicates the presence of potential hosts or prey.(6).
For the signals to be useful to the parasitoid, they should indicate the presence of 
a suitable host and be distinguishable from odors that are associated with non 
hosts.а Some of the chemicals disseminated from the infested plants are merely due 
to mechanical disruption of plant cells, and thus are not specific for herbivore 
damage(12).а Figure 2 illustrates the enormous variety in volatile blends that 
several different plant species release when damaged by herbivores.а In this case 
all of the depicted blends are the result of feeding damage inflicted by the beet 
armyworm Spodoptera exigua(7).
Until recently, evidence for herbivore specific cues has been limited.а Turlings et 
al. can now substantiate the variability of plant and host cues with their work onа 
Cotesia marginiventris.а C. marginiventris is a generalist that attacks the larvae 
of many Lepidoptera.а Research done by Turlings et al. on the foraging behavior ofа 
C. marginiventris has shown some ability to learn to distinguish between odors from 
different herbivores feeding on the same variety of plant. When an herbivore feeds 
on different structures of the same plant the odors emitted vary.а The increase inа 
response to host related odors after experience is greatest to the odors emitted by 
the plant-host complex that the female experienced.а The learning process that must 
be involved is triggered by a brief contact with host by-products and does not 
require a ctual contact with the host.а It has been shown that when females are 
given a longer experience period, including ovipositions, they did not appear to 
respond differently than females that had a much shorter experience without 
ovipositions.а The effect of the experience on the preference for host related odors 
was shown to last at least for several hours, and is likely to be an important 
factor determining host-searching behavior of C. marginiventris in the field(10).
It seems that signals would be most effective if emitted as soon as, or at least 
shortly after a herbivore starts damaging a plant.а Moreover, the volatiles would be 
most effective if they are emitted during the time of day when natural enemies are 
most likely to forage(6).а Work has been done to confirm whether or not the timing 
of volatile release is in tune with the parasitoids needs.а 
Several experiments were designed to monitor odor emissions by corn plants over a 
long period of time.а A method was used that allowed non-destructive collection of 
volatiles from growing plants.а Volatiles were sampled at periodic intervals 
throughout one or more photoperiods.а Volatiles were monitored at 2 hour intervals 
for up to 3 days.а Figure 3A represents the emission of several compounds that are 
representative of the total blend emitted by the corn seedlings.а Figure A 
graphically shows that the LOX products are released almost instantaneously in 
response to damage, but rapidly decrease after damage ceases.а Figure 3B represents 
the emission of terpenoids after the corn seedling was damaged and treated with 
The result was a delayed but dramatic increase in terpenoid emissions during daytime 
hours that was still detected on the third day after initial damage(6).а 
Although there is some delay, the plants seem to respond quickly enough for 
parasitoids and predators to effectively exploit the volatile signals.а The plants 
give off the strongest signals during the photoperiod when natural enemies tend to 
forage.а I nstead of the plants timing their responses to the active periods of 
parasitoids, it is more likely that one of the reasons natural enemies forage mostly 
during the day is because there are more visual and chemical cues available to them.а 
It is possible that the plants diurnal metabolism allows for volatile emissions only 
during the day.а On the other hand, the biology of night blooming plants suggests 
that there is no constraint on when volatiles could be emitted(6).
As herbivores have adapted to be inconspicuous to their natural enemies, it can be 
expected that they would emit very little in terms of odors that parasitoids could 
use to locate them.а Plants on the other hand benefit from the attraction of 
parasitoi ds, and may have developed means such as chemical signals to reveal the 
presence of herbivores.а It is unlikely that herbivore-damaged plants initiate the 
production of chemicals solely to attract parasitoids and predators.а The signaling 
role probably evolved secondarily from plant responses that produce toxins and 
deterrents against herbivores and antibiotics against pathogens(6).
It is clear that parasitoids most often utilize the cues from the host plant when 
foraging for potential hosts.а Insects overcome the constraints of the unreliable 
nature of the host plant cues by associative learning, and the ability to 
distinguish between herbivore damage plants and mechanically damaged plants.а The 
parasitoids are able to distinguish between "green leaf volatiles" and the blend of 
induced terpenoids emitted by herbivore damage.
The nature of the signals is obviously under the control of the plants.а Turlings et 
al. suspects that if the plant-produced chemicals are targeting the herbivores, then 
possible variations in chemicals that the plants produce may mainly result from 
different adversaries.а Turlings proposes that perhaps the plants do not need to 
release highly specific signals that differ when different herbivores attack it.а 
The plants so not necessarily suffer when natural enemies make "mistakes" and are 
attracted to the signals that are induced by herbivores they cannot attack.а As long 
as the "right" natural enemies are attracted as well, the signal has served its 
purpose for the plant.а It seems therefore up to the parasitoid to deal with some of 
the unreliable aspects of the signals(6).а In order to supplement the unreliable 
nature of the plant volatiles, the parasitoids often use other signals such as close 
range chemical contact, visual and vibrational cues in conjunction with herbivore 
induced volatiles from the host plant.ааааааааааааааааааааааааааааааааааааааааааа 
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