How Plants Can Help Us To Control Insects In Croplands

Abstract

Several plants, when injured by herbivore insects emit chemical signals to 
attract natural enemies of these insects. This phenomena was interpreted by many 
authors as a cry for help by the plants. Pare and Tumlinson (1997) suggest that 
mixtures of volatile terpenoids and other compounds that are released lead 
insect parasitoids, such as parasitic wasps and predators to distinguish between 
infested and non-infested plants - thus these compounds aid in location of hosts 
of prey. Turlings et al (1995) concluded that the clarity of the volatile 
signals is high. These signs are unique and produced in relatively large amounts 
by the plants. However, they argued that the specificity of the signals could be 
considered limited. In addition, they (the signals) are timed according to 
different factors.  McCall et al (1994) and Rose et al (1996), demonstrated the 
systematic release of infochemicals by cotton plants, while Turlings and 
Tumlinson (1992) discussed the same occurrence in corn plants. Loughrin et al 
(1994) discussed how the variation on the amount of compounds released depends 
on timing, arguing that this issue is strongly related to the herbivores feeding 
behavior.  In this paper I will discuss the evolutionary, ecological and 
chemical aspects of this interaction. Also, experimental approaches to determine 
the role of all agents and techniques used to identify the compounds involved 
will be quickly reviewed. Finally, the relevance of this knowledge, as it 
pertains to the crop protection strategies in the present and future, will be 
assessed. Scientists agree that considerable research will be needed to 
determine how best to use plant defense responses in insect control strategies. 


1. Introduction

Biological control of pests in agriculture is becoming more important due to the 
limitations for pest management related to ecological issues such as pollution, 
food contamination, and development of pest resistance. Insect behavior, and 
factors that mediate behavior must be understood to assure the success of such 
techniques. According to Tumlinson et al (1993), regardless of the approach used 
to employ parasitoid insects for pest control, ecological aspects involving 
their foraging behavior are important issues to be investigated.

It has long been noticed that several plants, when injured by herbivore insects, 
emit chemical signals (infochemicals) to attract predators of these insects. 
This phenomena was interpreted as a cry for help by plants. Pare and Tumlinson 
(1997) suggested that these chemical signals are mixtures of volatile terpenoids 
among other compounds that are released by plants, leading insect to distinguish 
between infested and non-infested plants. Thus these compounds aid in the 
location of hosts of prey (plants that are being damaged by herbivore insects). 

These parasitic and predatory insects prefer the clarity of these signals 
emitted by plants (indirect cues, though), instead of relying on specific 
chemical signals emitted directly by the herbivore insects, kairomones. This 
happens mainly due to the fact that the latter are not easily detectable at long 
distances by these predators. Turlings et al (1995) suggested that the clarity 
of volatile signals emitted by plants is high, as well as they are unique 
compounds produced in relatively large amounts. Volicitin, a key compound that 
induces plants to release these signals (infochemicals) when attacked by 
herbivore insects, was isolated and identified by Alborn et al (1997) from oral 
secretions of Beet Armyworm caterpillars.

Although many studies have been conducted on this specific field, not many 
papers exist summarizing the issue and providing an overall view of the matter. 
The organization of all available information in an objective and concise 
framework is important for planning future research. In the present review, I 
will discuss the evolutionary, ecological and chemical aspects of the 
interaction between insects and plants, with regard to this matter, summarizing 
all the pertinent facts. I will also provide a summary of the relevance of this 
knowledge, commenting on the future research that will be necessary to 
"unpuzzle" remaining questions.


2. Evolutionary and Ecological aspects

As Farmer (1997) appropriately states, herbivore insects and higher plants have 
been struggling for over 100 million years. Commonly in plants, damage by 
herbivore insects causes various changes in their composition, often referred as 
inducible defenses. These defenses may affect growth or reproduction in 
herbivore insects and frequently are represented by poisons, feeding deterrents, 
blocking proteins, cocktails of volatile compounds (indirect signals), and so 
forth (Edesltein-Kshet and Rausher, 1989).  Herbivore insects can often 
detoxify, sequester or bypass these inducible defenses. Some of the various 
volatile compounds (infochemicals) that are released by plants during the 
herbivore attack can attract parasitic insects. Whether this is the reason, is 
not yet known. What are the evolutionary and ecological aspects involved in this 
interaction among the three trophic levels (host plants, herbivore insects, and 
predatory insects)? This question introduces the present section of the review.

2.1. Plants releasing infochemicals

As stated previously, plants start a battle to defend themselves, immediately 
following injury by insects. Inbar et al (1998) pointed out that plant defensive 
systems primarily intend to control these insects, as well as, to avoid 
opportunist diseases that could take place (taking advantage of the mechanical 
damage that has just occurred). 

Tumlinson et al (1991) suggested that infochemicals are chemical signals used as 
a communication tool between organisms which help to locate food, mates, 
suitable site for their eggs, and progeny. Among the compounds produced by host 
plants in response to the herbivore insect attack, are the infochemicals that 
function as attractants for the natural enemies of these insects. These 
infochemicals will vary with the age, growth stage, part, strain or variety of 
the plant, as well as with the kind of insect that is feeding on the plant. In 
other words, this is a very complex system in which it is difficult to separate 
the infochemicals and assign their function (Tumlinson et al, 1991). 

MacCall et al (1994) accepted the challenge of studying all these infochemicals 
released by cotton plants, which they named herbivore-induced volatile 
emissions. They focused on investigating the collected volatiles from undamaged, 
freshly damaged (0-2 hours after feeding) and old damaged plants (16-19 hours 
after feeding), attacked by Corn Earworm caterpillars (Helicoverpa zea Boddie). 
According to them, healthy plants produce specific odors that are recognized by 
some herbivore insects. They pointed out that damaged plants, on the other hand, 
would produce anti-feedants (attempting to control the damage caused by the 
herbivore insects), and moreover, blends of volatile compounds that would 
attract the predators. They argued that this plant response would be only a 
general response against the herbivore insects (not attempting to call for 
predators), in which Turlings et al (1995) agree.  Finally, they concluded that 
significant differences regarding the composition of the volatile blends do 
exist among the three categories of plants. In other words, there are some 
compounds that are only released by the old damaged plants, and apparently they 
have special features as attractants of predators.

Turlings et al (1995), working with corn and cotton plants, inferred that the 
clarity of the infochemicals released by plants is high, meaning that they are 
produced in relatively large amounts and are not easily confounded with other 
odors. Regarding the specificity of these infochemicals, they concluded that it 
is limited. Agreeing with Tumlinson et al (1991), Turlings et al (1995) pointed 
out that, as the infochemicals vary with factors, they could not be considered 
exactly specific signals. This fact could cause some trouble to the predators, 
as they are not sure about the exact meaning of the cues. 


2.2. 
Where are these infochemicals produced, and from where are they released?


According to Ryan (1983), the compounds released by plants as a response to the 
herbivore insect attack (or to any other attack), could be produced or released 
at the site of the attack, as well as systemically by other parts of the plant. 
Moreover, the compounds could be produced at the site of the attack, transported 
to other sites, and released far from the site of the attack. McCall et al 
(1994) compared the composition of the volatile blends released by undamaged, 
freshly damaged, and old damaged plants on which insects were feeding; and 
concluded that significant differences do exist among the three categories of 
plants. In other words, there are some compounds that are only released by the 
old damaged plants, and the production of these compounds could be triggered by 
some special stimuli by herbivore insects.

Regarding the site from where these infochemicals are released, Turlings and 
Tumlinson (1992) pointed out the systemic release from the whole plant 
(including undamaged parts) in injured corn plants. Rose et al (1996), studied 
the release from undamaged leaves in cotton plants, concluding basically the 
same as Turlings and Tumlinson (1992). In other words, as soon as some leaves 
are damaged, they trigger the whole plant to a frenetic systemic reaction in 
response to it.

2.3. 
The Volicitin, a key compound

Tumlinson et al (1993), MacCall et al (1994), Turlings et al (1995), Rose et al 
(1996) and Pare and Tumlinson (1997) carried out experiments trying to determine 
why the composition of the volatile compounds released by plants changes 
drastically some hours after herbivores start feeding on them. They compared 
naturally damaged plants with artificially damaged ones, and figured out that 
the presence of the insects feeding on these plants is essential for the release 
of certain compounds that are responsible for the attraction of predators. Lead 
by the same curiosity, Alborn et al (1997) working with Beet Armyworm 
caterpillars, suggested that the incredible response of plants to the herbivore 
attack would be triggered by a substance encountered in the oral secretion of 
the insects. Rose et al (1996) supported the same idea one year before. After 
separating the secretion compounds and isolating the active ones by using 
chromatography techniques, these authors identified one single compound that 
would be responsible for the whole activity, by mass and infrared spectroscopy 
and by chemical transformations. The compound was named Volicitin (N-(17-
hydroxylinolenoyl)-L-glutamine). Finally, they synthesized the Volicitin, 
testing artificially damaged plants induced by synthetic Volicitin to see if 
they would emit the same blend of infochemicals as if they were damaged by 
insects and induced by their oral secretions, under natural conditions. After 
the bioassay procedure, they concluded that the Volicitin is indeed a key 
compound which regulate the tritrophic interactions among plants, herbivores and 
their predators. Later on, Farmer (1997), would call Volicitin as a new fatty 
acid-based signal discovered by Alborn et al (1997), and as "a lesson from the 
plant world" on how to deal with natural enemies. Furthermore, according to 
Alborn et al (1997), the presence of Volicitin in oral secretions does not 
depend on insect diet, and also, there is no evidence of enzymatic activity in 
eliciting volatile compounds, in this situation. The plants used in the 
experiment were cotton and corn seedlings. 

2.4. When are these infochemicals released?

Turlings et al (1995) also called the attention for the fact that the release of 
the infochemicals is timed - they tend to be released during the daytime, when 
natural enemies of the herbivore insects are foraging. Loughrin et al (1994) 
also investigated the diurnal cycle of emission of these infochemicals in 
herbivore-injured cotton plants. Rose et al (1996) suggested that the 
infochemicals in cotton plants would be released in higher quantities in the 
early afternoon.

This raises the evolutionary issue of how plants could have adjusted themselves 
to the predators schedule. Another theory is that predators could have evolved 
in order to forage during the time when infochemicals were released and, in 
addition, they could have visual stimuli to enhance their search. However it 
seems that this question will remain without an answer. Regarding this issue 
still, it must be clear that it is very difficult to understand and conclude 
about coevolution of plant-insects interactions based on studies with crops that 
have been modified by artificial selection (Turlings et al, 1995). 

2.5. 
Predators taking advantage of infochemicals

Pheromones, are particular infochemicals that are released within species for 
reproductive purposes. Furthermore, kairomones are another category of 
infochemicals used as a communication tool between two different species, 
favoring the receptor of the signal. This would be case in which the preys 
provide the predators (in this case the receptors) infochemicals (kairomones) 
with specific information about their location (the prey's location) and the 
characteristics of themselves. However, herbivore insects adapt to be 
inconspicuous to their natural enemies, as one would expect. By doing this, it 
turns out that the amounts of odors released by them are very small compared 
with the infochemicals released by plants on which they are feeding. Thus, 
predators somehow have to be able to guide themselves by the infochemicals 
released by plants, although they do not provide them with quite specific 
information.

2.6. Solving the specificity problem

As stated previously, potential host insects tend to escape the detection by 
kairomones, due to the fact that nature imposes a variety of selection pressures 
on them. The most inconspicuous are the ones that subsist. Therefore, indirect 
cues are the only information available to the foraging parasitoid female, at 
least while it is far from its host insect. The infochemicals produced by the 
plants are fundamental cues that tell the parasitoids that certain habitat is 
likely to contain suitable hosts (Tumlinson et al, 1993). However, this 
information is still vague to solve the situation.

Intriguing learning abilities were mentioned by Turlings et al (1995) and other 
authors, and studied by Tumlinson et al (1993). They  pointed out that predators 
get the first information about their hosts when they first emerge, at the 
beginning or their life cycle. As suggested by the researchers, they will never 
forget this information which will lead them in the future, when they need more 
specific information about the hosts for their eggs.  Furthermore, these authors 
described how the wasp (parasitic insects) will find their hosts by associating 
odors released by them (feces, and other by-pass products) with the odors 
released by their host plants. The level of sophistication for this ability 
surprised the authors while they made use of interesting bioassay procedures 
described by Tumlinson et al (1993). Thus, wasps learn visual, chemical, and 
other cues, showing an amazing system for detecting and tracking their prey - 
solving the specificity problem.


3. Chemical aspects

The volatile compounds detected from cotton plants that were fed by Beet 
Armyworm larvae include Monoterpenes, Sesquiterpenes, Homoterpenes, Lipoxygenase 
products, Indole, among others (Pare and Tumlinson, 1997). On the other hand, a 
very specific chromatographic profile of the volatile compounds collected from 
Beet Armyworm caterpillar feeding on corn is provided on Turlings et al, 1990's 
paper. The description or the discussion of the chemical processes involved in 
the separation and identification of the compounds goes beyond the objectives of 
the present paper.


4. Comments about some experimental approaches

All experimental approaches described in all the papers that were reviewed apply 
the postulates of Chemical Ecology in a very responsible manner. In other words,  
bioassays are in general planned and conducted respecting the most acceptable 
theoretical reasoning. However, when studying the function of Beet Armyworm oral 
secretions, the researchers "collected the oral secretions by squeezing third to 
fifth instar Beet Armyworm caterpillars that had been fed corn seedlings, 
causing them to regurgitate" (Alborn et al, 1997). This method could be 
questioned based on the fact that the natural feeding behavior of this insect 
was neglected. Furthermore, it appears that almost all the papers that were 
found in the literature are somehow linked to the same group of researchers. 
This fact could lead to a biased point of view of the real scenario.


5. 
Relevance and Future Research

Many researchers agree that biological control is frequently cheaper, safer, and 
more reliable than chemical control (Tumlinson et al, 1993). Led by this 
knowledge, the aim of this paper was to demonstrate that inducible defenses in 
plants (in this case represented by infochemicals) may aid in controlling the 
dynamics of herbivore populations in agricultural systems, by affecting the 
ecological relations among insects communities. 

The successful establishment of any biological control strategy will be enhanced 
if parasitoid females are able to find their hosts more quickly. Recognizing the 
importance of this fact, Tumlinson et al (1993) stated that the knowledge of the 
behavior and factors mediating behavior of insects is becoming essential for the 
success of any program of biological control. Furthermore, manipulating the 
behavior of parasitoids to improve their foraging effectiveness is clearly the 
key issue related to this matter.

For this reason, the role of infochemicals must be better understood. More 
knowledge about the injury-dependent production of infochemicals by plants may 
pinpoint to new possibilities for biological control of pest insects (Turlings 
et al, 1990). Insect training techniques appear to be very important once these 
individuals present so fascinating learning abilities. 

Among other issues that also deserve careful attention, are the better knowledge 
elicitors as Volicitin, as well as the determination of precise timing for all 
interactions (McCall et al, 1994). Considerable research will have to be 
conducted to determine how best to use plant defense responses in insect control 
strategies, by manipulating the dynamics of insect populations in controlled 
agricultural systems.


6. References:


Alborn, HT; Turlings, TCJ; Jones, TH; Stenhagen, G; Loughrin, JH; Tumlinson, JH
(1997). An Elicitor of Plant Volatiles from Beet Armyworm Oral Secretion. 
Science v. 276 p. 945-948.

Alborn, HT; Turlings, TCJ; Tumlinson, JH (1993). An elicitor in caterpillar oral
secretions that induce corn seedlings to release parasitoid attractants. Plant 
Signals in Interactions with other Organisms p. 256-257.

Edelstein-Keshet, L; Rausher, MD (1989). The effects of inducible plant defenses 
on herbivore populations. 1. Mobile herbivores in continuous time. The American 
Naturalist v. 133 p. 787-810.

Farmer, EE (1997). New Fatty Acid-Based Signals: A lesson from the plant world. 
Science v. 276 p. 912-913.

Loughrin, JH; Manukian, A; Heath, RR; Turlings, TCJ; Tumlinson, JH (1994).
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McCall, PJ; Turlings, TCJ Loughrin, J; Proveaux, AT; Tumlinson, JH (1994).
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Inbar, M; Doostdar, H; Sonoda, RM; Leibee, GL; Mayer, RT (1998). Elicitors of 
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Pare, PW; Tumlinson, JH (1998). Cotton volatiles synthesized and released distal
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Roachell W (1996). Parasitoid host selection: host and host food-plant cues.
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Rose, USR; Manukian, A; Heath, RR; Tumlinson, JH (1996). Volatile
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Ryan CA (1983). Insect-induced chemical signals regulating natural plant 
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Tumlinson, JH; Lewis, WJ; Vet, LEM (1993). How parasitic wasps find their hosts.
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