Understanding Semiochemicals with Emphasis on Insect Sex Pheromones in Integrated Pest Management Programs
| Hollis M. Flint1 and Charles C. Doane2 | ||
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1USDA-ARS-WCRL 25934 E. Calle del Sud |
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Introduction
Semiochemicals (Gk. semeon, a signal) are chemicals that mediate interactions
between organisms. Semiochemicals are subdivided into allelochemicals and pheromones
depending on whether the interactions are interspecific or intraspecific, respectively.
(For a discussion of terminology, see Anonymous 1981.) Allelochemicals, then, are
chemicals that are significant to individuals of a species different from the source
species. Allelochemicals are subdivided into several groups depending on whether the
response of the receiver is adaptively favorable to the emitter but not the receiver
(allomones), is favorable to the receiver but not the emitter (kairomones) or is favorable
to both emitter and receiver (synomones). Within both allelochemicals and pheromones it is
sometimes useful to refer to chemicals as arrestants, attractants, repellents, deterrents,
stimulants or other descriptive terms. These terms can indicate what behavior is involved
in the response such as a feeding stimulant or flight arrestant. Pheromones (Gk. phereum,
to carry; horman, to excite or stimulate) are released by one member of a species
to cause a specific interaction with another member of the same species. Pheromones may be
further classified on the basis of the interaction mediated, such as alarm, aggregation or
sex pheromone. It is the sex pheromones of insects that are of particular interest to
agricultural integrated pest management (IPM) practitioners.
The concept of IPM is based on the recognition that no single approach to pest control
offers a universal solution, and that the best crop protection can be provided by a fusion
of various tactics and practices based on sound ecological principles. Pheromones are a
commonly used component of many insect IPM programs. (For an up-to-date discussion of IPM,
see Dent, 1993 and Anonymous, 1995.)
The existence of pheromones has been known for centuries, apparently originating in observations of mass bee stinging in response to a chemical released by the sting of a single bee. The first isolation and identification of an insect pheromone (silkworm moth) occurred in 1959 by German scientists. Since then, hundreds, perhaps thousands of insect pheromones have been identified by increasingly sophisticated equipment. Today we have a much clearer view of the limitations and possibilities associated with insect pheromones in IPM programs. The two primary uses of insect pheromones are for detection and monitoring of populations and for mating disruption. These uses take advantage of sex pheromones on which a vast majority of insect pests rely to mediate reproduction.
Uses of Pheromones in IPM
Detection and Monitoring. The principle use of insect sex pheromones is
to attract insects to traps for detection and determination of temporal distribution. In
most instances, it is the males who are responders to female-produced sex pheromones. Trap
baits, therefore, are designed to closely reproduce the ratio of chemical components and
emission rate of calling females. Ideally, a trap bait should uniformly dissipate its
pheromone content over time and not permanently retain or degrade the pheromone in the
process. Trap baits of many designs have been tested over the years, but the hollow
polyvinyl plastic fiber (emit from open ends), closed hollow fiber and bag (emit through
walls) and laminated plastic flake (emit through walls and exposed edges) are commonly
used today. Trap design is also critical to effective use of traps for monitoring insect
populations. Traps vary in design and size dependent on the behavior of the target
insects. Consistent trapping protocols are essential for population evaluations, spray
thresholds, and year to year comparisons. The information from trap catches can be very
useful for decision making on insecticide applications or other control measures. For
example, trap catches may indicate a loss of effect of pheromone on mating disruption and
the need to reapply a pheromone treatment. Careful monitoring and experience in
interpreting collected data are important for success. Traps may also be placed with the
objective of destroying males for population control.
Male annihilation is trapping carried to a seemingly logical conclusion. Place enough
traps, catch enough males, and leave the females of the species without mates. This
approach has been used against pink bollworms in an isolated area of Arizona with low
numbers of overwintering moths. A rate of 5 traps per acre was used and the traps were
composed of Styrofoam cups containing oil to provide larger capacity for dead moths. These
traps were placed on row centers to avoid the cultivator and never serviced again. The
grower community paid for this program for a few years, but results were difficult to
prove because a control area was not available. Calculations by Dr. Edward Knipling (USDA
retired) indicated that almost all (95%+) male pink bollworms would have to be destroyed
before they could mate in order to exert significant population control. Any untrapped
males simply mate more frequently. Mating disruption does not depend on traps for control,
although traps are frequently used to monitor the extent of mating disruption in the
population. Failure to trap males is taken as an indication that males are unable to find
females which may or may not be true. Thus, trap data must always be related to actual
levels of crop infestation.
Mating Disruption. With the commercial availability of insect sex
pheromones for several agricultural pests in the 1970's, scientists and entrepreneurs
turned their attention to mating disruption as a "biorational" approach to
insect control. In theory, mating disruption may be accomplished in two principle ways:
false trail following or confusion. False trail following results from placing many more
point sources of pheromone (hollow fibers, flakes or other point sources) per acre than
the anticipated numbers of females in the crop. The odds of males finding females at the
end of the pheromone trail must be greatly reduced. Emission of pheromone is relatively
low from each source such that a downwind trail is created and not lost in a background of
released pheromone. Males following these trails are thought to spend their mating
energies in pursuit of artificial pheromone sources. Pink bollworm males were early
observed trying to mate with hollow fiber pheromone sources in treated fields. Thereafter,
commercial pink bollworm pheromone products were applied in stickem containing small
amounts of a contact insecticide. The resulting attract-and-kill formulations (another
form of male annihilation) were viewed as a subversion of the pheromone by purists, but in
practice the damage was limited to the target species. However, the effectiveness of the
added insecticide is largely unknown under field conditions. Growers endorsed the idea
that a dead male is better than a confused one. A further combination of pheromones and
insecticides is occasionally encountered. Dual applications of pheromone and full strength
insecticides (either separately or in tank mixes) are applied with the idea of increasing
insect flight activity and thus increasing the chance of insecticide exposure. Full
strength applications of pheromone are generally used for this method. The greater the
amount of pheromone applied and the greater the release rate, the more likely males are to
be confused in the fog of ambient pheromone.
Male confusion is thought to be the result of ambient pheromone concentrations
sufficient to hide the trails of calling females (large doses from diffuse sources such as
microcapsules or larger doses of pheromone in point source dispensers such as tie-on
polyethylene ropes). Added to the effect, or indeed the effect, is the adaptation of
antennal receptor sites and/or habituation of the insect's central nervous system.
Specific receptor sites on the antennae respond to only the pheromone molecules
(individual component molecules appear to have individual receptor sites on antennae).
When a receptor site is continually activated by high ambient concentrations of
pheromones, the resulting electrical signal diminishes (measured by an
electroantennogram). The receptor site becomes unresponsive and the insect becomes
navigationally blind. When the insect's central nervous system is inundated with signals
from the receptor sites it becomes habituated: no longer able to provide the directed
behavior. All of the above are, to some degree, based on known neurophysiology, but
exactly what proportion of each occurs in a given situation can only be guessed. The net
result of confusion is that the male is unable to orient to any pheromone source and
follow the upwind trail to a mate. For a current summary of theory and application of
pheromones for control of Lepidopterous pests, see Cardé and Minks (1995).
Present commercial formulations of pheromones for both trap baits and mating disruption
mimic the natural chemical blends of females as clearly as possible. Most insect sex
pheromones are multicomponent with precise ratios of components which may be expensive to
manufacture. Thus, insect sex pheromones and products containing pheromones, are
commercially available primarily for insects of economic importance. Fortunately, there is
hardly an insect species of agricultural importance, among the Lepidoptera at least, for
which there are not some pheromone products available.
It is impossible to cover here all the insect pests for which IPM programs using
pheromones are recorded. We have selected agricultural pests for discussion that we are
familiar with or for which information is readily available.
Specific Uses of Pheromones in IPM
Photograph: Boll weevil, Anthomonus grandis.
The boll weevil, Anthonomus grandis Boheman, has been a primary pest of cotton
since its introduction to the United States in 1892. Numerous methods have been used to
control weevils, but the idea of eradication has always had advocates. It was not until
the early sixties that it was shown that the male boll weevil produces a sex pheromone in
its frass that is attractive to females. This pheromone was also shown to act as an
aggregating pheromone for both sexes (primarily in early and late season). The four
components of the pheromone were identified and synthesized by the late 1960's and called
grandlure. Formulations that were attractive as trap baits made survey and monitoring
possible over wide cotton growing areas of the cotton belt.
In 1978, an eradication program for the boll weevil began which continues today.
Basically, the program includes: 1. In-season control using insecticides. 2.
Reproduction-diapause control in early and late season to reduce the numbers of weevils
entering cotton fields each spring. 3. Survey and monitoring with pheromone-baited traps.
4. Area-wide insecticide treatment of cotton at first pin-head flower bud ("hostable
square" stage) in the spring. As of this date, December 1995, boll weevils have been
eradicated from much of the eastern cotton belt and programs are underway in central
states including Mississippi, Louisiana, and Texas. Because small cotton fields are the
norm in much of the cotton belt, the use of up to 1 trap per acre (along field borders) is
required to detect extremely low residual populations. Detection of a single weevil
results in more intense trapping. Capture of a second weevil is considered evidence of a
possible reproducing population and spraying is initiated. Pheromone-baited traps are
placed on millions of acres of cotton to monitor new and old program areas. During the
1995 season, the program consumed 2 million traps and 25 million trap baits--the largest
program of its kind in the world. Malathion (ULV) is the current principle insecticide
used in program-directed spraying. The boll weevil eradication program is jointly funded
by federal, state, and grower money and has saved billions of dollars in weevil control
over its lifetime. Just as importantly, the use of insecticides to control boll weevils,
ca. 40% of the total U. S. consumption, is being reduced. Complete eradication of boll
weevils from the United States is projected for approximately the year 2010. Eradication
from Mexico undoubtedly will be approached similarly. See Dickerson et al. (1987) for an
outline of the boll weevil eradication program.
Photographs: Pink bollworm. Pectinophora gossypiella and twist-on
spiral mating disruptant pheromone dispenser.
Efforts to control the pink bollworm, Pectinophora gossypiella (Saunders), by
mating disruption began with the sex attractant "hexalure" in the early 1970's.
The discovery of the pink bollworm sex pheromone in 1973 led to the first successful
commercial formulation in 1978 (see review by Baker et al. 1991). The pheromone, a two
component mixture of Z, Z- and Z, E-7,11-hexadecadienyl acetate (called gossyplure in
commercial products), has appeared in a variety of aerially applied formulations including
hollow fibers, flakes, microcapsules, and in hand-applied twist-tie ropes and twist-on
spirals. Original applications utilized 0.75 to 1.5 g AI/acre in several thousand point
sources and were applied several times during early to mid-season while recent
hand-applied formulations utilized ca. 30 g AI/acre and were applied once. These are known
as false-trail following and confusion methods, respectively. All formulations are to be
applied at first flower bud ("pin-square" or about 8 true leaf stage cotton)
which is the earliest fruiting form in which the pink bollworm can reproduce. Applications
at first flower bud are made against the lowest seasonal (over-wintered) populations, an
aid to efficacy.
Commercial use of pheromone in IPM programs for control of the pink bollworm is widely
used in Arizona. The current and perhaps most successful demonstration of the value of
this approach is the Parker, AZ, program on ca. 25,000 acres of cotton along the Colorado
river in the northwest corner of the state. Deemed to be a somewhat isolated area of the
northern extreme of pink bollworm overwintering, the area growers have supported a
systematic approach fashioned after the successful boll weevil eradication program. The
area-wide program has used selected commercial formulations (including dual applications
with insecticide) to reduce pink bollworm populations each year during the past 5 seasons.
The results have been so satisfactory that very little control for pink bollworm is
presently needed in the program areas.
Systematic IPM programs using pheromone to control pink bollworm are also in use in
India and Pakistan, but attain the greatest acreage in Egypt. Pheromone treatments
totaling a hundred thousand acres or more were used in Egypt during the 1995 season.
Published reports indicate the program of several years is expanding and has produced
control of pink bollworm comparable to conventional insecticides. The use of pheromone in
Egypt is under state control and is applied to selected large areas of cotton. An overall
view of cotton pest management is provided by Luttrell et al. (1995).
Spruce Bark Beetle. A historically interesting demonstration of IPM
methods on a forest insect occurred in Norway. An outbreak of spruce bark beetles, Ips
typographus L., killed millions of spruce trees annually in Norway in the late
1970's and early 1980's. The three-component pheromone, identified in 1977, was used in
600,000 stove pipe traps in south Norway in a Government funded cooperative program with
40,000 forest owners. The aggregation pheromone attracts both sexes and the traps, shaped
like a tree trunk, have the capacity to hold thousands of beetles. Pheromone trap baits
were either plastic bags or laminated plastic tape containing 1580 mg of active
ingredients with a service life of about 2 months (the main flight period). The baits were
used either on standing trap trees, subsequently cut and removed, on insecticide-sprayed
logs, or in traps. These techniques represent trap crop, attract-and-kill, and
annihilation, respectively! Traps were placed in areas of high infestation and were
combined with cultural practices such as cleanup of slash and dead trees, logging of
mature (susceptible) stands, and quick removal of unbarked cut trees from the forest.
Total trap capture in 1980 was estimated from sample captures to be 4.5 billion beetles.
Pheromone-baited traps quickly replaced trap trees because traps were cheaper and resulted
in the removal of more beetles. Trap trees had to be removed from the forest at the proper
moment to avoid emergence of new beetles and were also shown to remove large numbers of
parasites and predators at the same time. The objectives of the program were met when the
beetle populations were reduced to levels too sparse to overcome healthy trees. The major
component of the continuing program is maintenance of good cultural practices and
pheromone trapping in outbreak areas.
Codling Moth. The codling moth, Cydia pomonella L., is one of the
most destructive insects on pome fruit throughout the world. It is responsible for most of
the insecticide sprays on apples and pears in the Pacific Northwest. Eradication or
suppression of this pest over large areas would allow noninsecticidal control measures to
be used on this and other species. Currently, 2 million pounds of insecticides are used
for control of pome fruit pests in the northwest. Resistance to Guthion, the standard
insecticide for codling moth has increased to the point that growers are forced to use 5-6
sprays instead of 1 or 2 per season. This change has created the necessary economic
impetus to fund IPM programs. In 1994, pilot tests of suppression tools including
biological control, sterile insect releases, orchard sanitation, and mating disruption
were begun in the states of Oregon, Washington, and California. Funding for these pilot
tests were initially through the USDA's Agricultural Research Service, but AgCanada and
grower groups are expected to participate in the program. Ultimately, the program will be
area wide and grower dictated and funded.
A rope-type pheromone dispenser is used at a rate of 1000 ropes per ha, about 4 ropes
per tree. Each rope contains a total of 1 mg of the 3 component pheromone (all straight
chain alcohols). The ropes are placed two each in upper and lower tree canopy and the
orchards monitored using wing-type traps containing 10 mg baits which seem to be
detectable by males above the ambient pheromone background. Orchards with high
infestations are sprayed with Guthion to first reduce the populations. Problems
encountered thus far in the pilot test and in commercial use of pheromone for mating
disruption are infestations along the borders of treated orchards. These localized
infestations are thought to be due to uneven pheromone concentration in multi-layered
upwind edges of orchards. Also, incoming mated females from other areas are difficult to
control. A major component of the IPM program for apples and pears is the treatment or
elimination of abandoned trees and home owner's backyard trees. The area wide IPM program
for codling moth is projected for implementation in 1997. Information on this program may
be obtained from Dr. C. O. Calkins, Yakima Agricultural Research Laboratory, 5230 Konnowac
Pass Road, Wapato, WA 98951. See Bloomers (1994) for a summary of IPM methods in European
apple orchards.
Tomato Pinworm. Pheromones have played a major role in controlling infestations
of the tomato pinworm, Keiferia lycopersicella (Walsingham), a primary pest of
tomatoes. Larvae attack leaves, but economic damage is greatest when they enter the fruit.
Development of a control system using sex pheromone for control of the tomato pinworm was
initiated in 1979, soon after the identification of the pheromone as a 96:4 mix of E and
Z-4-tridecenyl acetate. A hollow fiber formulation was first successfully developed in
Mexico's Culiacan Valley. Commercial use of the pheromone increased during the 1980's as
the pinworm became increasingly resistant to insecticides. Problems with insecticide use
were several: control became more expensive as repeated applications of chemical
insecticides failed to control the pest, insecticide residues resulted in condemnation of
tomatoes intended for shipment into the United States and outbreaks of secondary pests
were often triggered by repeated applications.
By the end of the decade, growers of both stake and processed tomatoes in Mexico had
changed completely to IPM programs using mating disruption for control of the pinworm.
This pheromone is especially intriguing because it can be used successfully against heavy
infestations of the pinworm. Most pheromone programs require that initial applications
start when the pest is at a low numerical density. Traps and lures are also used widely to
detect moth emergence cycles so that timely applications of pheromone or insecticides can
be applied. For discussion, see Jenkins et al. 1991.
European Corn Borer. The European corn borer, Oestrinia nubilalis (Hübner), is an important pest of corn, cotton, sorghum, and vegetable crops in the
eastern United States. The European corn borer has two generations per year in most of the
United States which limits population growth and places a premium on control of the first
generation. The pheromone of the European corn borer was identified as a mixture of Z- and
E-isomers of 11 tetradecenyl acetate in the early 1970's. Interestingly, three distinct
populations of European corn borer exist (sympatrically in some areas), separated by
ratios of the two isomers of their pheromone. The Z and E strains utilize predominantly
these isomers in their pheromones and hybrids utilize intermediate ratios. Pheromone traps
are used to monitor populations with large cone traps catching approximately seven times
as many males as wing traps which rely on a limited amount of sticky surface. Therefore,
trap type, ratio of Z- and E- isomers and lure strength are critical for consistent
results in monitoring the European corn borer. Unfortunately, adjacent areas may require
different trap baits for optimum catches. Current practice for IPM management include
population monitoring with pheromone traps and judicious use of biorational materials such
as the various B.t. products and insecticides.
Miscellaneous Uses of Pheromones in IPM
Trap crops for insect control are occasionally employed although suitable target
insects are limited. Early season boll weevils can be concentrated in cotton planted to
reach the susceptible square stage ahead of the main crop and then selectively sprayed
with insecticide. A strip of cotton the width of a single spray swath of tractor or
aircraft is used adjacent to the fields to be protected. The addition of boll weevil
aggregating pheromone in the cotton, aids in concentrating weevils for killing. This
approach, including pheromone dispensers, was used in localized areas of high weevil
infestation near Phoenix, AZ in the 1980's. The outcome is unrecorded, but the program was
grower supported and funded.
Recently (Salom et al. 1995), an inhibitor-based tactic was demonstrated to suppress
infestations of the southern pine beetle, Dendroctonus frontalis Zimmermann. The
southern pine beetle uses a variety of semiochemicals to mediate mass attack on host pine
trees. Two aggregation pheromones, frontalin and trans-verbenol, function in directing
other beetles to join in the mass attack of a host tree that is necessary for successful
colonization. Once the tree is overcome, no further beetles are needed and two
anti-aggregation pheromones, endo-brevicomin and verbenone, are released to divert beetles
to other trees. Two or three polyethylene bag dispensers, each containing 5 ml of
verbenone (6 week service life), were placed on trees in several freshly infested areas in
Virginia. Unbaited sticky screen traps (1m2) were suspended 4.5 m above the
ground between trees to monitor beetle movement (flight traps) or placed around tree
trunks (landing traps). Similar but untreated infestations were used as controls. The
applications of verbenone were moderately to fully effective in stopping the progression
of infestations. The pheromone treatments had no effect on sampled natural enemies at the
infestation sites. The verbenone suppression tactic can be applied to small to
moderate-sized infestations of southern pine beetle. combined with other control measures,
anti-aggregation pheromones are appropriate for use in forest insect IPM programs.
Conclusions
The use of semiochemicals, including pheromones, that modify insect behavior is still a
developing area of science. The awareness of environmental and safety hazards, associated
with insecticides, coupled with the technology to measure their presence, have lead to
increasing restrictions on their use. The costs of introducing new insecticides or even
re-registration of existing insecticides, is time consuming and expensive. These problems
with insecticides have driven the search for new control technology. Pheromones and other
behavior-modifying chemicals found naturally in the environment, offer non-insecticidal
alternatives which are being commercially pursued by both new companies and established
giants of the insecticide industry.
An added impetus to the use of semiochemicals for insect control is the commitment of
the United States government, through the USDA, EPA and FDA facilities, to attain IPM
systems on 75% of total crop acreage by the year 2000. This IPM initiative redirects and
combines USDA and Land Grant university programs into a single coordinated effort to
address important pest control problems. A measurement of the success of introducing IPM
programs will be the negative impact on pesticide use and adoption of alternative control
technology. Several area-wide pest management programs have been initiated which focus on
key pests where existing technologies (pheromones, biocontrols, resistant plants) are
available. As part of the USDA IPM initiative, a number of IPM development and
implementation teams have been formed. Subject areas for which IPM implementation is
underway include corn and soybeans, vegetable crops, grapes, apples, landscaping,
potatoes, wheat and barley, tomatoes, cucurbits, and greenhouse systems, among others. For
team leaders and general information, contact Dr. R. M. Faust, National Program Leader,
Field and Horticultural Crop Entomology, Building 005, BARC West, Beltsville, MD 20705,
telephone 301/504-6918, FAX 301/504-6231.
The recognition that alternative control technologies must be applied in coordinated
programs covering large areas is now understood. Thus, there is need for close association
between scientists who develop control technologies and a larger group of program managers
and their field staffs. This concentration of forces and technologies on the battlefield
decides the ultimate form of IPM. The history of insect control clearly demonstrates that
complete reliance on a new control technology soon leads to some form of resistance.
Hence, the IPM strategy of applying all the available control measures with thoughtful
intent to preserve the value of each will be necessary. Semiochemicals, and particularly
insect sex pheromones, are a useful part of many detection, monitoring, and control
programs for agricultural crops.
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