Understanding Semiochemicals with Emphasis on Insect Sex Pheromones in Integrated Pest Management Programs
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.
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.
Photograph: Pink bollworm. Pectinophora gossypiella
Photograph: 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.
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.
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.
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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- Baker, T. C., R. T. Staten, and H. M. Flint. 1991. Use of pink bollworm pheromone in the southwestern United States. pp. 417-436. In Behavior Modifying Chemicals for Insect Management. Ridgeway, R. L., R. M. Silverstein, and M. N. Inscoe [eds.]. Marcel Dekker, New York, NY.
- Bloomers, L. H. M. 1994. Integrated pest management in European apple orchards. Ann. Rev. Entomol. 39:213-241
- Cardé, R. T. and A. K. Minks. 1995. Control of moth pests by mating disruption. Ann. Rev. Entomol. 40: 559-585.
- Dent, D. 1993. Integrated insect pest management. pp. 439-533. In Insect Pest Management. Dent, D. [ed.]. CAB International, Wallingford, UK.
- Dickerson, W. A., R. L. Ridgeway, and F. R. Planer. 1987. Southeastern boll weevil eradication program, improved pheromone trap, and program status. pp. 335-337. Proc. Beltwide Cotton Research and Production Conference, National Cotton Council, Memphis, TN.
- Jenkins, J. W., C. C. Doane, D. J. Schuster, J. R. McLaughlin and M. J. Jimenez. 1991. Development and commercial applications of sex pheromone for control of the tomato pinworm. pp. 269-280. In Behavior Modifying Chemicals for Insect Management. Ridgeway, R. L., R. M. Silverstein, and M. N. Inscoe [eds.]. Marcel Dekker, New York, NY.
- Luttrell, R. G., G. P. Fitt, F. S. Ramalho, and E. S. Sugonyaev. 1994. Cotton pest management: Part 1. A Worldwide Perspective. Ann. Rev. Entomol. 39: 517-526.
- Salom, S. M., D. M. Grossman, Q. C. McClellan and T. L. Payne. 1995. Effect of an inhibitor-based suppression tactic on abundance and distribution of southern pine beetle (Coleoptera: scolytidae) and its natural enemies. J. Econ. Entomol. 88: 1703-1716.