BEHAVIORAL MANIPULATION METHODS FOR INSECT PEST

October 17, 1996 16:49 Annual Reviews chapter-06

Annu. Rev. Entomol. 1997. 42:123–46Copyright c© 1997 by Annual Reviews Inc. All rights reserved

BEHAVIORAL MANIPULATIONMETHODS FOR INSECTPEST-MANAGEMENT

S. P. Foster and M. O. HarrisThe Horticulture and Food Research Institute of New Zealand, Mt. Albert ResearchCentre, Private Bag 92169, Auckland, New Zealand; e-mail: [email protected];[email protected]

KEY WORDS: behavior, attractants, repellents, stimulants, deterrents

ABSTRACT

We discuss methods using stimuli to manipulate behavior of a pest for the purposeof protecting a valued resource. The methods are divided into two categories:those that manipulate behavior over a long distance, e.g. volatile chemicals,visual, and auditory stimuli, and those that manipulate behavior at a short distance(< 1 cm), e.g. involatile chemicals. Particular emphasis is placed on methods thathave been developed through studies of pest behavior and on combining stimulito increase efficacy. Future prospects for behavioral manipulation methods inpest management are discussed.

INTRODUCTION

An insect is considered a pest if it threatens a resource valued by humans,including human health. Protection of a resource from a pest is usually achievedby poisoning the pest with a toxic pesticide, but it can also be achieved bymanipulating a behavior of the pest. The manipulation of a pest’s behavior toprotect a resource is not a new concept. The practice of trap cropping, i.e. usinga sacrificial resource for the pest to attack, in order to protect a valued resource,has been known for centuries (70). However, in the last 30 years or so, largelydue to improvements in analytical techniques and an increased desire to reducethe reliance on broad-spectrum insecticides, there has been increased interestin behavioral manipulation for pest management.

Virtually all methods of pest management involve some changes in pest be-havior, whether intentional or not (52). In this review, we restrict our discussion

1230066-4170/97/0101-0123$08.00

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to examples in which pest management is achieved through deliberate manip-ulation of a pest’s behavior. For the purpose of this review, that manipulationis defined as the use of stimuli that either stimulate or inhibit a behavior andthereby change its expression. This definition excludes some areas in whichchanges in pest behavior are advantageous to pest management, notably thoseresulting from sublethal effects of toxic chemicals or substances that induce agross change in physiology (52, 65) and those that merely consider the pest’sbehavior, as in planting a crop out of synchronization with the pestilential be-havior (1). Additionally, because of limitations in space, we focus on methodsthat use the stimuli that have been defined and reproduced artificially. Conse-quently, we do not discuss methods in which resources (particularly plants) areused to manipulate pest behavior, e.g. breeding for antixenosis (42), trap crop-ping (70), and intercropping (3). Although these methods are not discussed, theprinciples underlying these methods are essentially the same as those discussedin this review.

BEHAVIORAL MANIPULATION METHODS

There are three principal elements of a behavioral manipulation method: a be-havior of the pest, a means by which the behavior is manipulated appropriately,and a method that utilizes the behavioral manipulation for protection of a re-source from the pest. In theory, any behavior of any stage of the pest can bechosen, provided that its manipulation protects the resource. Intuitively, onemight expect that manipulation of a pestilential behavior (e.g. feeding on theresource) or a behavior closely related to the pestilential behavior (e.g. findingthe resource) is more likely to be useful for pest management than manipulationof behaviors unrelated to the resource (e.g. mating). Successful manipulationof the pestilential behavior will ensure protection of the resource; successfulmanipulation of an unrelated behavior may reduce the local population but stillnot protect the resource because of immigration of outside populations into thearea being protected, as can occur in the mating disruption method for moths(27). In practice, however, the criterion by which a behavior is usually chosenfor manipulation is not its relationship to the pestilential behavior but rather theavailability of an appropriate means for its manipulation.

The behavior of an insect results from the integration by its central nervoussystem of a variety of inputs that derive from stimuli acting on exteroceptors(which sense events external to the insect), enteroceptors (which sense theinternal physiological state of the insect), and proprioceptors (which sense therelative positions of parts of the body) (62, 82, 134). To manipulate a behaviorone must change either the inputs or the processing of those inputs by thecentral nervous system. At present the latter approach is generally inaccessible

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BEHAVIORAL MANIPULATION METHODS 125

for effecting deliberate manipulation of a behavior, although it may occur insome instances as a sublethal effect of a toxic insecticide (65). Thus, insectbehavior generally is manipulated through inputs to the behavior and morespecifically through the stimuli that generate these inputs (62).

The choice of a stimulus to use for behavioral manipulation is usually de-pendent upon a number of attributes including the following.

1. Accessibility. The stimulus must be suitable for presentation in a form thatthe insect can perceive.

2. Definability and reproducibility. The more precisely that the stimulus canbe defined, the more precisely it can be reproduced artificially.

3. Controllability. The ability to control various parameters of a stimulus,including intensity and longevity, will give greater control in a behavioralmanipulation.

4. Specificity. The more specific a stimulus is to a particular behavior of apest, the more likely it can be used to manipulate that behavior. Conversely,a stimulus that is ubiquitous in the environment is unlikely to be usefulfor manipulating specific behaviors unless its intensity or quality can beperceived by the insect above the background level. For example, “super-normal” visual targets (i.e. objects that reflect high ratios of stimulatory toinhibitory wavelengths of light) are used to outcompete the natural visualbackground reflecting a lower ratio of stimulatory to inhibitory wavelengths(124).

5. Practicability. Environmental hazards and cost of protecting a resourcemust be within practical limits. For example, chemicals that are persistentand have high mammalian toxicities may protect an edible resource butrender it useless for human consumption.

In light of these desirable attributes, it is not surprising that the use of stimuliacting on exteroceptors predominates over the use of stimuli acting on ente-roceptors (internal stimuli) (62). For the most part, internal stimuli are inac-cessible for behavioral manipulation (see below) and are difficult to define andcontrol. The listed attributes also support the much greater use of chemicalscompared to other external stimuli used in behavioral manipulation. In additionto the listed attributes, chemicals are used more often because of their involve-ment in many insect behaviors (e.g. 19, 26), their familiarity because of wideuse in pest control, and the advances over the last 30 years in techniques toanalyze chemicals involved in insect behavior.

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In contrast to work on chemical stimuli, the investigation of visual stimulifor behavioral manipulation has been much less. This is probably due in largepart to the lack of specificity of many visual stimuli involved in behaviors (e.g.image flow during flight), as well as the general impracticality of changingvisual stimuli to effect behavior. For example, it is difficult to change the visualproperties of plants to make them less attractive to insects, although gibberellicacid has been used to keep grapefruit green and less attractive than yellow fruitto Caribbean fruit fly females (53). However, visual stimuli are important, ifoften unrecognized, components of many behavioral manipulation methods, asin the effects of color and form of odor-baited traps in eliciting landing andcatch of a pest (46, 113).

For behavioral manipulation, only two classes of mechanical stimuli war-rant mention, tactile and acoustic. Tactile stimuli are perceived during contactand are important in the acceptance of hosts, as in the ovipositional behaviorof female insects (63). Difficulties in definition and reproduction have limitedtheir use in behavioral manipulation. In contrast to tactile and other mechanicalstimuli, acoustic stimuli can be defined precisely. However, the use of acousticstimuli is relatively uncommon among insects. Their use in behavioral manip-ulation is limited to pests that exhibit long-range phonotaxis. Acoustic stimuli,generated naturally or electronically, have been used to attract mole cricketsand field crickets and have also been shown to be useful for attracting malemosquitoes of the genusAnopheles. To date, the high cost of sound-generatingequipment has limited the application of acoustic stimuli to monitoring pestpopulations (156).

Although external stimuli are most commonly used, it is sometimes possibleto change internal inputs to a behavior, at least at a gross level (62). For example,mated female insects often receive different mechanical and hormonal internalstimuli that cause them to behave differently than virgin females (149).

Although defining and reproducing stimuli generally allows greater flexibilityand control in behavioral manipulation, it is by no means essential. Undefinedor poorly defined stimuli, in the form of natural objects such as plants, frequentlyare used to manipulate behaviors (see Introduction), an approach that does notrequire extensive research to define stimuli. The resulting lack of definition,however, also means that there is little control over the stimuli, and if the methoddoes not work, there is little recourse to constructive change.

Manipulation of insect behavior through stimuli must be conducted within thecontext of a method to be useful (Figure 1). A method consists of a strategy forbehavioral manipulation and the mechanism that implements the strategy. Forexample, in the attract-annihilate method (see below), the strategy is to attractpests to a site and remove them from the environment, and the mechanism maybe a trap or a surface coated with a deleterious substance (toxin or pathogen).

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Figure 1 The behavioral manipulation method concept illustrated using the example of an attract-annihilate method.

EXAMPLES OF BEHAVIORAL MANIPULATIONMETHODS

In this section we review behavioral methods that have been used for the con-trol of insect pests. We have classified methods into those that act over along distance (finding-type behaviors) and those that act at a short-distance(acceptance-type behaviors). To describe the types of stimuli, especially chem-icals, we use the common terms of attractant and repellent for long-distancestimuli and stimulant and deterrent for short-distance stimuli. We recognizethat these terms merely describe the end result of a behavioral response to thestimulus (82), but we use them for brevity and because often a behavior has notbeen studied in sufficient detail or within a broad enough context to determinethe actual behavioral response to the stimulus used.

In choosing examples, we have not limited ourselves to practical successesbut also include methods that have only been tested experimentally. That isbecause the adoption of a method is often determined by such extrinsic factorsas the availability of other pest management methods and the prevalence of otherpests, rather than effectiveness of the method per se. Consequently, changes in

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economics or the loss of other pest management methods may make a methodthat is considered impractical today practical in the future.

Stimuli that Act Over Long DistancesATTRACT-ANNIHILATE The attract-annihilate method is by far the most widelyused behavioral manipulation for pest management. The strategy of the methodis simple: attract the pests to a site where as many of them as possible can beremoved from the environment (93). The behavioral manipulation involves along-distance attractant, and the mechanism consists of a device whereby theattracted pests are killed or trapped.

This method has been used for many pests whose behavior includes long-distance orientation, usually flight but also walking, as in certain species ofcockroaches (133). The most commonly used attractants are volatile chemicals,but visual stimuli are also used (intentionally or incidentally) and auditorystimuli could also be used (156).

Chemical Stimuli Sex pheromones have been identified for a large numberof insect pests, particularly Lepidoptera (7). These chemicals have a num-ber of useful attributes for the attract-annihilate method, including specificity,eliciting long-distance responses, and longevity in the field. However, be-cause most sex pheromones are produced by females and elicit responses frommales, they have been used primarily in the mating disruption method (seebelow) or for monitoring (157) rather than in the attract-annihilate method.Removal of adult males, unless at a very high proportion of the population,is unlikely to have a large impact on the size of subsequent generations com-pared to removal of females (93). Nonetheless, there are a few examples ofeffective control by mass-trapping based on sex pheromones, including the cit-rus flower mothPrays citri on lemons in Israel (143), sporadic outbreaks ofthe gypsy moth in the United States (84), and some stored-product pests inwarehouses (44, 147, 148). Sex pheromones have also been used as attractantsto facilitate contact with and dispersal of pathogens in pest populations (e.g.111, 137).

The limitation of a sex pheromone attracting only males can be overcome bycombining it with an attractant for females. Theoretically, such a combinationshould be more effective in the attract-annihilate method than either attractantalone (14). A combination of the sex pheromone, which attracts males, and afood lure (a mixture of phenethyl propionate, eugenol, and geraniol), which pre-dominantly attracts females, has been used against the Japanese beetle,Popilliajaponica. The combination trapped more males and females than the two at-tractants did when used separately (89). Visual stimuli are also important forP. japonica, and the catch of beetles is greater in white traps than those of othercolors (88).

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Aggregation pheromones attract both sexes and in some species immatures,e.g. nymphs of the German cockroachBlatella germanica(131). Their abilityto attract females makes these pheromones well suited for the attract-annihilatemethod (93). Aggregation pheromones have been used successfully for control-ling various Coleoptera, including the cotton boll weevil,Anthonomus grandis,in the United States (60) and bark beetles in North America and Europe (13,25, 93).

The olive fruit fly,Dacus oleae, a major pest of olives in the Mediterraneanregion, has been controlled as effectively as with insecticides by an elaboratemass-trapping method (59). Females of this species produce a blend of com-pounds that attracts males over a distance (97). One of these compounds, 1,7-dioxaspiro[5.5]undecane is also produced by males. The (R)-(−) enantiomerof this compound attracts only males, and the (S)-(+) form of this compoundelicits a response that appears to be aggregation by females (58). The methodinvolves a combination of attractants and stimulants on an insecticide-treatedwooden board, which includes a racemic mixture of spiroacetal, a food attrac-tant (ammonium salts) for females, a hygroscopic substance (glycerol) becausethe flies are attracted to moisture, and a feeding stimulant (sugar) that is usedto increase contact with the insecticide.

The screwworm fliesCochliomyia hominivoraxandCochliomyia macellariaare major pests of livestock in tropical America, and recentlyC. macellariahasalso been recognized as a pest in North Africa (48). These flies, which lay theireggs in wounds, are attracted to carrion, and raw meat (often a combination ofliver and sodium sulfide) is used in traps to control or monitor them (22). Anumber of the chemicals in rotting meat that attract screwworm flies have beenidentified and used as an attractant, originally called swormlure, for screwwormcontrol (31, 76). The most effective formulation, now known as swormlure-4, contains ten components, including butanol, several organic acids, phenol,cresol, indole, and dimethyl disulfide (95).

In addition to their use in traps, swormlure and its derivatives have been usedin two other attract-annihilate methods to control or eradicate screwworms,as well as in the sterile male technique (see below). The screwworm adultsuppression system (SWASS) consists of a pelletized formulation containing thechemical lure, food (dried blood), a feeding stimulant (sugar), and an insecticide(32). This combination attracts the flies and induces them to feed, therebyacquiring a lethal dose of insecticide. The pellets are generally dropped fromaircraft.

In the SWASS method, pellets must be dropped twice weekly for effectivecontrol because of their short life under field conditions (3–5 days). In addition,although the pellets restrict insecticide usage, they pose a threat to the environ-ment, particularly around waterways and inhabited areas. To overcome these

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limitations, a protected bait station utilizing the same combination of methodsas the SWASS was developed. The longevity of these stations is about 45 to 60days (33).

A chemical need not be a natural stimulus in a behavior to function as an at-tractant. Many so-called moth sex attractants, which attract male moths but havenot been identified in conspecific females, have been found by screening largenumbers of related chemicals (7). A group of chemicals that has proven very ef-fective as attractants for certain species of tephritid flies are the male lures. Themost important of these chemicals are methyl eugenol, 1-(p-acetoxyphenyl)-butan-3-one (cue-lure), and t-butyl 4 (or 5)-chloro-2-methyl-cyclohexanoate(trimedlure), which attract males of various species of Tephritidae of the OldWorld tropics and subtropics and Oceania. Despite a great deal of investigation,these chemicals have no known role in the natural biology of the flies, yet theyelicit much greater responses than any natural sex pheromone in the respectivespecies of flies (35).

Methyl eugenol was first used in a male eradication program for the Orientalfruit fly, Dacus dorsalis, by Steiner and coworkers on the island of Rota (northof Guam) in the Marianas (141). Essentially, they absorbed a mixture of methyleugenol and insecticide (naled) onto cane-fibre squares and either threw themout of an airplane in uninhabited areas or placed them in trees in village areas.This method, either alone or in combination with another such as the sterilemale technique, subsequently has been used a number of times to control oreradicate populations of Oriental fruit fly in the Marianas (140), the UnitedStates (35), and Japan (86, 151). It also was used to eradicate an infestation ofDacus zonatusin California in 1987 (35).

Food baits are also useful for monitoring or controlling tephritids. Proba-bly the most important of these have been the protein hydrolysates of corn,soybeans, or yeast. Microbial fermentation of these baits produces volatilechemicals that attract a range of tephritids. They have the advantage over malelures of attracting females as well as males (28). Protein-hydrolysate-baitedtoxic baits have been used to eradicate the Mediterranean fruit fly,Ceratitiscapitata, in the mainland United States during the later part of this century (28,72, 142).

Visual Stimuli Visual stimuli alone are much less commonly used in attract-annihilate methods than chemical stimuli. Many hemipterans as well as speciesin other orders are attracted to light in the green-yellow region of the spectrum.This attraction has been utilized in the development of yellow sticky traps formonitoring a number of pests, including the citrus blackfly,Aleurocanthus wog-lumi (64); the tarnished plant bug,Lygus lineolaris(120); the beet leafhopper,Circulifer tenellus(102); and the greenhouse whitefly,Trialeurodes vaporari-orum(51), in commercial orchards or greenhouses.

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Samways (132) attempted to use attraction to green-yellow light to develop anattract-annihilate method for the citrus psylla,Trioza erytrae, a vector of citrusgreening disease in southern Africa. The method consisted of a combination ofperimeter sticky traps, utilizing a plastic sheet with high reflectance in the yellowregion and low reflectance in the blue, and pesticide-treated trap trees. Althoughfewer insects were caught inside the protected area than outside, there was nosignificant difference between mean population levels over the period of theexperiment. In part, this was due to the very low population numbers of the pestduring the trial, as shown by trap catches, and also perhaps because of conditionsthat suppressed dispersal. This method needs to be tested more rigorously, underdifferent environmental conditions and at different population levels, in orderto determine its suitability for control of this and perhaps other pests.

Visual and Chemical Stimuli Visual stimuli are used most frequently in com-bination with chemical stimuli, enhancing the efficacy of a method over the useof either stimulus type alone. Even in methods that do not purport to use visualstimuli, such as sex pheromone-baited traps, the visual stimuli of traps are im-portant (see 46). Tsetse (Glossinaspp.), which are the vectors of the protozoansthat cause trypanosomiases in sub-Saharan Africa, including human sleepingsickness and important animal diseases, provide one of the best examples of theuse of both visual and chemical stimuli in an attract-annihilate method. Attract-annihilate methods are particularly suitable for control of tsetse because of theadenotrophic viviparity and low reproductive potential of each female, whichcommonly produces less than ten offspring. The host-finding behavior of tsetseis influenced by visual stimuli, including shape, orientation, brightness, con-trast, movement, and color (2, 30). Traps using only visual stimuli, such as thebiconical trap, are used for control of these flies (107). Tsetse also respond tohost odors, some of the attractive components of which include CO2, 1-octen-3-ol, butanone, acetone, and various phenols (30). The addition of odor (acetoneand CO2) to the biconical trap doubled catches over a non-odor-baited trap (45).

In recent years, control of tsetse has relied increasingly on the use of odor-baited black cloth targets coated with insecticide (152). The combination ofvisual and olfactory stimuli appears to concentrate a fly’s movements towardthe target, as well as to increase its chances of landing on it (146). Recently,the efficacy of odor-baited tree stumps with a nearby insecticide-treated nettingwas investigated for tsetse control; the method was effective with short trunksbut less so with taller, upright trunks, which tsetse avoid (153). An attract-annihilate target method utilizing both chemical and visual stimuli similar tothat used for tsetse flies is being developed for screwworm control (54).

An elegant variant of the attract-annihilate method has been devised for con-trol of the apple maggot fly,Rhagoletis pomonella. Females of this speciesfind host trees and suitable oviposition sites on apples using a combination of

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host odors and visual stimuli (6, 121). Initially, a sticky red wooden sphere(slightly larger than an apple) was developed for the control of this fly. Hang-ing these sticky spheres on each tree in an apple orchard gave good protection(< 1% damage) of fruit fromR. pomonella(118). The trap was improvedthrough identification of odors from apples that attract the flies (43). Plac-ing the sticky spheres baited with butyl hexanoate on the perimeter trees ofa small orchard block gave protection equal to that of nonbaited spheres onevery tree of the block (122). Principally because of difficulties with handlingthe sticky spheres and the need to recoat them regularly to maintain efficacy, apesticide-coated target was developed. In addition to the combination of odorand visual stimuli the red spheres are coated with a feeding stimulant (cornsyrup), which increases contact of the flies with the insecticide; without thefeeding stimulant, most of the flies do not remain on the sphere for sufficienttime to be exposed to a lethal dose of insecticide. The targets are as effec-tive as sticky spheres as long as they are dipped in sugar solution after eachrainfall (40).

DISRUPTING BEHAVIOR USING ATTRACTANTS AND REPELLENTS Disrupting be-havior with stimuli that either elicit or inhibit orientation is also effective at longdistances. In practice, only attractant and repellent chemicals have been used.The distinction between attractants and repellents is less clear than the namessuggest. Most stimuli that attract will repel at higher concentrations (11). Stim-uli that repel a pest may elicit orientation in the same or other species (110). Forexample, the insect repellent N,N-diethyl-m-toluamide (deet) will attract themosquitoAedes aegyptiat sufficiently low concentrations (85). These terms,particularly “repellent,” are often used problematically in the literature, becausethe actual effect of the chemical is surmised from the end result of the behavior,which could be influenced by short-range stimuli such as deterrents. Never-theless, attractants or repellents are generally identified as such in behavioralmanipulation methods, and we follow conventional usage.

Attractants Most work on the use of attractants to disrupt a finding behaviorhas focused on mate location, particularly of moths, in the so-called mating dis-ruption method (27, 105, 128, 129). Large amounts of synthetic sex pheromoneare distributed with the aim of preventing males from finding females. Thismethod has been used successfully for control of such herbivorous pests as thepink bollworm,Pectinophora gossypiella, on cotton; the Oriental fruit moth,Grapholita molesta, on stone fruits; the tomato pinworm,Keiferia lycopersi-cella, on tomatoes; and the currant clearwing,Synanthedon tipuliformis, onblackcurrants (see examples in 27, 128, and references therein). In virtually allcases where the method has been attempted, disruption of mating has been atleast partially achieved in the treated area. However, the success of the method

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for management of a given pest depends to a large extent on its biology andparticularly on the potential for immigration of mated females from outside thetreated area (27).

A number of possible behavioral modes of action have been suggested formating disruption with synthetic pheromones (15, 27), including diminution ofresponse due to sensory adaptation or habituation, arrestment of upwind flightat high concentrations, shifting the rhythm of response to females, chang-ing the fine structure of or camouflaging a natural plume, outcompeting fe-males, and causing an imbalance of sensory inputs by altering the perceivedblend. In spite of the large amount of work on mating disruption of moths,as well as the considerable volume of work on the actual behavioral mech-anisms used by male moths in response to pheromone (11), “the extent towhich any of these mechanisms actually participate in achieving mating dis-ruption remains speculative, because either direct field experimentations havefailed to explore all the mechanisms or, more likely, such tests have not beenattempted” (27).

An interesting variant of the mating disruption method is used for controlof the pink bollworm in California: an insecticide, permethrin, is added to thesticker used to attach the pheromone formulation to the leaves of the plant. Thiscombination is thought to increase the control of bollworm over the pheromonealone (12).

Another example of an attractant used to disrupt a finding behavior has beenprovided by the navel orangeworm,Amyelois transitella, a pest of almonds inCalifornia. Both volatile chemicals emanating from almond fruits and frass oflarvae feeding on almonds stimulate oviposition by female navel orangewormand provide an effective attractant in monitoring traps (36, 38). Chemicalsfrom almond oil elicit upwind flight over relatively long distances (>2 m) (112).Spraying a formulation of 5% crude almond oil in water on almond trees sup-pressed egg deposition on egg traps and reduced the infestation of mummy nuts(unharvested, previous year’s nuts) in a California orchard (154). Althoughthe behavioral mode of action that led to the decrease of oviposition was notdetermined, the volatility of the active component(s) suggests that the methoddisrupted the orientation and finding behavior of the females. Almond oil incombination with an insecticide also shows promise as an attract-annihilatemethod for the navel orangeworm (112).

Repellents The strategy for using repellents is, generally, to stop a pest fromfinding a valued resource. Useful repellents can be derived from natural sourcessuch as insects (e.g. defense secretions), or they may be purely artificial as in thecase of most insecticides (37, 110). Most work on the practical use of volatilerepellents has been to protect humans from insect bites, particularly from those

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insects such as mosquitoes and blackflies that are vectors of diseases (136). Ofthese chemicals, the best known is deet, which is used as a repellent for a widerange of insects (130).

Repellents to protect crops, except those also with general insecticidal ac-tivity such as nicotine, have received little attention in contrast to the greatamount of investigation into the chemical basis of plant resistance against in-sects (126). Verbenone, a known inhibitor of aggregation in bark beetles, andpine oil repel colonization of forest trees or logs by various species of barkbeetles (41, 83, 108). Interestingly, pine oil has also been used in the laboratoryto prevent oviposition by the onion fly,Delia antiqua, on treated onion halves(73), although the behavioral mode of action (repellency or deterrency) was notdetermined. Another repellent that has been used to protect a plant resource isthe chemical (E)-(β)-farnesene, a major component of alarm pheromones of anumber of species of aphids (116). Laboratory and field trials showed that thiscompound increased contact with toxic chemicals and fungal pathogens by theaphidMyzus persicae(56, 57).

Stimuli Acting at Close DistanceAfter arriving at a resource, an insect is likely to contact additional (to thoseperceived at greater distances) stimuli. These stimuli can either stimulate abehavior, keeping the insect at the resource, or inhibit that behavior, resultingin rejection of and possibly movement away from the resource. Virtually allthe short-range stimuli used in behavioral manipulation are chemicals.

STIMULANTS Most known stimulants are involved in either feeding or ovipo-sition, primarily the former (10, 126). Advantages of stimulants include in-creasing exposure to toxins that must be ingested and applicability to a widerange of pests, as in the case of sucrose. Feeding stimulants also are oftencommon carbohydrates, proteins, or fats (10) that are easily obtained and rela-tively inexpensive, whereas oviposition stimulants can be highly specific, evenamong pests that threaten same resource (71), and expensive.

Feeding stimulants are especially useful in conjunction with toxins (10),because they can increase contact that may be suppressed if the pest respondsto the toxin by ceasing to feed, thus avoiding a lethal dose (e.g. endotoxinsof Bacillus thuringiensis). They also have been used in combination withattractants (attract-annihilate method) using commercially available stimulants,e.g. protein hydrolysate in the eradication of tephritid fruit flies (28) and sugarsfor control of flies around animal rearing facilities (114).

Other feeding stimulants in development for use in toxic baits are the cucur-bitacins. These oxygenated tetracyclic triterpenoids found in many species ofCucurbitaceae stimulate compulsive feeding in adults of a number of species

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of diabroticite beetles (101), including corn rootworms,Diabroticaspp., whichare important pests in the United States. Cucurbitacins are obtained by growingplants with high concentrations and harvesting, drying, and grinding them to apowder that is combined with an insecticide as bait. In small trials, such baitshave been effective in reducing populations of several species of corn rootworms(92, 100). Because cucurbitacins act only as feeding stimulants, chemical at-tractants have been sought to increase the number of rootworms finding thebaits (90, 92, 100). Rootworm attractants appear to be more species-specificthan the feeding stimulants but have improved the efficacy of poison baits insome studies (91, 100, but see 92).

Oviposition stimulants have not yet been used commercially for pest control,but such a method is suggested by the work of Unnithan & Saxena (150). Inthis study, oviposition by the sorghum shootfly was stimulated on nonhostplants (corn) by applying an acetone extract of sorghum. In small field trials,the extract diverted oviposition from the sorghum. Although this effect wasattributed to an oviposition stimulant, it may have acted as contact stimulant, along-distance attractant, or both.

DETERRENTS A deterrent is a chemical that inhibits behavior, such as feedingor oviposition, when applied to a site where such behavior normally occurs (21).In pest management, a deterrent is applied directly to a resource to prevent orreduce the effects of a pestilential behavior such as feeding. Efficacy dependson the physiological state and behavioral responses of the pest during initialand subsequent encounters with the deterrent (4, 75, 123). If a pest stays on orreturns to the resource, protection may break down in several ways, of whichthe most important is desensitization (47, 123). Numerous pest insects havebeen shown to lose their responsiveness to deterrents after repeated exposureand after increasingly long periods of deprivation of feeding or ovipositionalsites (4, 20, 135).

Protection also may break down when the resource is not uniformly treatedwith the deterrent, and the pest can move to an untreated part. For examples,plants can grow after a deterrent has been applied and therefore present the pestwith unprotected surfaces over time, except in the case of systemic deterrents(109). However, movement of a pest from a deterrent-treated site to a deterrent-free site can be exploited for pest management if the movement brings thepest to a nonvalued part of the resource or an area that has been treated with apesticide. This strategy was used against larvae of the mustard beetle,Phaedroncochliereae, which were deterred from feeding by application of extracts ofplants in the genusAjuga to the young leaves at the top of mustard plants;beetles moving down to feed on older leaves were controlled by an insectgrowth regulator (55).

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Because deterrents repress behaviors, oviposition or feeding deterrents areoften found by studying the chemistry of plants on which pests do not feed oroviposit (20). Many researchers see deterrents as more important in host plantpreferences than stimulants (21). Frass of species other than the target that feedon similar host plants are another potential source of deterrents. The cabbageroot fly, Delia radicum, did not lay eggs on cauliflower plants sprayed with anextract of the frass of caterpillars of the garden pebble moth, with sinapic acidas the active component (77).

Deterrents found in extracts of the Neem tree have attracted great interest inrecent years, especially azadirachtin (8, 106). Neem extracts and azadirachtinaffect behavior, growth regulation, ovarian development, fecundity, and fertilityin insects. Neem chemicals may control pests that will not consume them bydeterrent effects. Lepidoptera are most sensitive to azadirachtin, with feedingdeterred at< 1–50 ppm (106). The dual action of deterrence and toxicity and themany pest species that are controlled by one or both of these actions contributeto interest in Neem chemicals.

Only a few plant-derived feeding deterrents in addition to Neem have beentested in small glasshouse or field plots. Polygodial, a plant-derived dialdehydicsesquiterpenoid in the drimane series, is a feeding deterrent for various lepi-dopteran pests such asSpodopteraandHeliothisspecies (24) and for the aphidM. persicae(50). InM. persicae, deterrence of feeding decreased spread of per-sistent and semipersistent plant viruses. In field trials, polygodial significantlyreduced transmission of barley yellow dwarf virus by the aphidRhopalosiphumpadi and increased yields of barley from 3.83 to 5.22 tonnes per hectare (39).Fatty acids, such as dodecanoic acid (68) and plant-derived oils (158), are alsounder examination as feeding deterrents against aphids and have shown somepromise in small trials.

The deterrent properties of fungicides have been known for many decadesand were discovered through observations of pest populations feeding on treatedand untreated plants (20, 144). When organotin and copper compounds usedas fungicides to protect potatoes against disease were replaced with systemicfungicides, populations of Colorado potato beetle increased substantially (74).The fungicides were subsequently shown to control beetle populations bydeterring feeding. When sprayed on crops in field trials, these compoundshave successfully controlled various species of Lepidoptera, Coleoptera, andHymenoptera (20). Despite their success in pest management, organotins fellfrom favor in the late 1970s because of environmental concerns (20). Copperfungicides are still used as feeding deterrents and have been proposed for man-aging pesticide resistance in Colorado potato beetles (61).

Field trials on oviposition deterrents are limited to a single species, the cherryfruit fly, Rhagoletis cerasi. A host-marking pheromone put on the fruit by the

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female after she oviposits deters oviposition by conspecifics on the same fruit.An extract of the pheromone sprayed on cherry trees reduced fruit infestationby wild R. cerasilarvae tenfold (79, 80). Trials with the synthetic pheromonehave given similar reductions in fruit infestation (5). The recent identificationand synthesis of host-marking pheromones from the eggs of butterflies in thegenusPieris(23) and the relative stability of these compounds present a similaropportunity for using oviposition deterrents to protect cabbage crops from thesepests (135).

COMBINING DETERRENTS AND ATTRACTANTS/STIMULANTS Several authorshave suggested that the efficacy of a deterrent-based method may be increasedif used in combination with another method that attracts the pest to a nonvaluedresource in a stimulo-deterrent diversion (103, 104) or push-pull (125) strategy.The combination of methods might overcome such difficulties with deterrentsas desensitization and untreated areas of the resource.

The stimulo-deterrent strategy (SDD) was conceived for insect herbivoresbut is applicable to any pest and any resource type. To date, it has only beentested against a small number of herbivores in small field or glasshouse trialsand has yet to be used commercially. The onion flyD. antiquacan be deterredfrom laying eggs on seedling onions by cinnamaldehyde and stimulated tolay eggs on worthless cull onion bulbs that are planted in the same field (34).In large-scale field trials (JR Miller & RS Cowles, personal communication)using microencapsulated cinnamaldehyde as the deterrent and cull onions asthe stimulant, the SDD strategy appeared to give good protection for the firstfew weeks following application. Control subsequently broke down due to theshort lifespan of the deterrent formulation. Moths of the genusHeliothisweredeterred from ovipositing on cotton by azadirachtin and stimulated to ovipositon pigeon pea or maize crops (127, 125). Although the two methods havenot yet been combined, researchers in Britain (138) have shown in separatefield trials that the adult pea and bean weevil,Sitona lineatus, can be deterredfrom feeding on a leguminous crop by neem oil and attracted into other cropfields using aggregation pheromones. As suitable deterrents and stimulants areidentified, it seems likely that such combined behavioral manipulation methodswill be developed for a wider range of pests and resources.

Internal StimuliOne exception to the generalization that internal stimuli are inaccessible formanipulating behavior is the sterile male technique, in which large numbersof sterile males are released to mate with wild females. The mating inducesmany of the same internal inputs in the females as in those mated to normal,fertile males. These internal inputs induce a number of behavioral changes in

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the female. Most usefully, the female becomes refractory to further matings,and in species in which the female mates only once, will remain refractorypermanently and hence never be fertilized.

The sterile male technique has been used successfully in eradication pro-grams, usually in combination with other methods such as poison baits, againstisolated or incipient populations of economically severe pests where the riskof reintroduction is low, such as the primary screwworm in North and CentralAmerica (17, 87) and various tephritid fruit flies (69, 72, 78, 139). The methodcan be used for control through ongoing population suppression, but the highcost of producing the large numbers of high-quality insects needed to swamp oroutcompete wild males generally makes this approach uneconomical (9, 49).Besides a large rearing program producing high-quality insects, the methodrequires an ability to sterilize large numbers of insects (usually by X-ray orγ -ray exposure), and an effective monitoring system that can be used to detectthe pests and to estimate the size of the pest population.

FUTURE PROSPECTS

Many future developments in behavioral manipulation will be based on currentresearch, especially in-depth studies on behaviors in a wider range of insectspecies. Besides increasing our understanding of insect behaviors, such studiesshould also provide knowledge of more stimuli for behavioral manipulation.Given the present emphasis on chemical stimuli and their advantages, as well asthe increasing sophistication of chemical techniques, a wider variety of chemi-cals that mediate behavior presumably will be identified and used. For example,3-methylindole, a recently identified attractant/oviposition stimulant for gravidfemaleCulex quinquefasciatusmosquitoes may be used for management ofthis pest (18). Research on physiological processes involved in insect behav-iors may characterize more internal stimuli and lead to new methods for usingthem, e.g. insect neuropeptides (81, 98, 99). Advances in biotechnology mayalso play a part. Microorganisms could be genetically engineered to provide amore economical production of semiochemicals than synthetic chemical routes(115), and resources such as crop plants could be modified to introduce novelstimuli or enhance stimuli already associated with them.

Whether behavioral manipulation methods will have a greater impact in pestmanagement than they do at present will depend on their perceived advantagesand disadvantages relative to other methods. Pest management worldwide iscurrently dominated by broad-spectrum toxic chemicals. The limited adop-tion of behavioral manipulation methods suggests that perceived advantagessuch as specificity and low toxicity are generally not sufficient to overcomedisadvantages such as cost and inability to control other pests, compared to

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the advantages and disadvantages of chemical pesticides. However, becauseof health and environmental concerns, such as recent initiatives in Europe toreduce agricultural pesticide usage by 50% (96), and pesticide resistance, thelong-term future of such pesticides is somewhat uncertain, and opportunitiesfor behavioral manipulation methods may increase.

Behavioral manipulation methods may be subject to some of the same prob-lems as conventional pesticides. Many chemicals proposed for use in behavioralmanipulation, particularly plant-based feeding deterrents, have not been thor-oughly tested for toxicity against a wide range of organisms. Also, some naturalenemies use the same stimuli to find pests as the pests use to find their hosts.Thus, behavioral manipulation methods (particularly attract-annihilate) usingthese stimuli could have adverse affects on natural enemies. Finally, althoughresistance of pests to behavioral manipulation has not been observed (66, 67),individual variation in behavioral components (e.g. 29, 52, 94, 155) indicatesa potential for changes that would result in resistance (117).

CONCLUSIONS

Behavioral manipulation methods for pest management can be developed in avariety of ways, from detailed studies of behavior in the laboratory and field(e.g. apple maggot fly) to nearly serendipitous observations of pest populationsin the field (e.g. effects of fungicides on Colorado potato beetle). However,without a thorough understanding of the behavior and ecology of the pest (119),the chances for developing a successful method other than by serendipity areslight, and the ability to modify and refine the method to enhance its efficacyfor pest management is limited.

The behavior of insects is influenced by many stimuli, both external andinternal (62, 82), and failure to account for the effects of these stimuli mayresult in apparent variable results with a behavioral manipulation. Internalstimuli related to different physiological (16) and experiential (123, 145) statesare important sources of behavioral variability and should not be ignored. Theexamples of the excellent studies on tsetse and other flies testify to the benefitsof identifying and using multiple types of stimuli in behavioral manipulationfor pest management.

Understanding the range of behaviors exhibited by a pest throughout its lifecycle assists identification of those most suitable for manipulation, as well asallowing one to develop elaborate combinations of behavioral manipulations.Examples of these more elaborate methods include combinations of distinctbehaviors with a common behavioral mechanism, e.g. sex pheromone andfood odors in traps for the Japanese beetle (89); combinations of complementarybehaviors, e.g. the attractant and feeding stimulant used in toxic baits for olive

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fruit fly (59); and combinations of converse behaviors, e.g. the stimulo-deterrentdiversion strategy for herbivores (104, 125).

There have been a limited number of succesful examples of behavioral ma-nipulation methods in pest management. Whether these and new behavioralmanipulation methods continue to occupy a relatively small niche or play amajor role in pest management is likely to depend on the amount of researchon the causes of insect behavior and the development of creative methods forutilizing the results of this research.

ACKNOWLEDGMENTS

The authors thank Drs. Martin Birch, Tibor Jermy, Jim Miller,Arpad Szentesi,Tristram Wyatt, and Mr. Julio Rojas for comments on the manuscript. Thiswork was supported by a grant (Contract No. C06512) from the New ZealandFoundation for Research, Science, and Technology.

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Annual Review of Entomology Volume 42, 1997

CONTENTSJ. S. KENNEDY (1912–1993): A Clear Thinker in Behavior's Confused World, John Brady 1

ADAPTATIONS IN SCALE INSECTS, Penny J. Gullan, Michael Kosztarab 23

ECOLOGY AND EVOLUTION OF GALLING THRIPS AND THEIR ALLIES, Bernard J. Crespi, David A. Carmean, and, Thomas W. Chapman 51

DIPTERA AS PARASITOIDS, Donald H. Feener Jr, Brian V. Brown 73

WILD HOSTS OF PENTATOMIDS: Ecological Significance and Role in Their Pest Status on Crops, Antônio R. Panizzi 99

BEHAVIORAL MANIPULATION METHODS FOR INSECT PEST-MANAGEMENT, S. P. Foster and, M. O. Harris 123

VISUAL ACUITY IN INSECTS, Michael F. Land 147

INTERACTIONS AMONG SCOLYTID BARK BEETLES, THEIR ASSOCIATED FUNGI, AND LIVE HOST CONIFERS, T. D. Paine, K. F. Raffa, T. C. Harrington 179

PHYSIOLOGY AND ECOLOGY OF DISPERSAL POLYMORPHISM IN INSECTS, Anthony J. Zera, Robert F. Denno 207

EVOLUTION OF ARTHROPOD SILKS, Catherine L. Craig 231

INSECTS AS TEACHING TOOLS IN PRIMARY AND SECONDARY EDUCATION, Robert W. Matthews, Lynda R. Flage, and, Janice R. Matthews 269

LIFE-STYLES OF PHYTOSEIID MITES AND THEIR ROLES IN BIOLOGICAL CONTROL, J. A. McMurtry, B. A. Croft 291

PHOTOPERIODIC TIME MEASUREMENT AND RELATED PHYSIOLOGICAL MECHANISMS IN INSECTS AND MITES, Makio Takeda, Steven D. Skopik 323

SYSTEMATICS OF MOSQUITO DISEASE VECTORS (DIPTERA, CULICIDAE): Impact of Molecular Biology and Cladistic Analysis, Leonard E. Munstermann, Jan E. Conn 351

HOST PLANT INFLUENCES ON SEX PHEROMONE BEHAVIOR OF PHYTOPHAGOUS INSECTS, Peter J. Landolt, Thomas W. Phillips 371

MIGRATORY ECOLOGY OF THE BLACK CUTWORM, William B. Showers 393

PHYLOGENY OF TRICHOPTERA, J. C. Morse 427

THE BIOLOGY, ECOLOGY, AND MANAGEMENT OF THE CAT FLEA, Michael K. Rust, Michael W. Dryden 451

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BEHAVIOR AND ECOLOGICAL GENETICS OF WIND-BORNE MIGRATION BY INSECTS, A. G. Gatehouse 475

BIONOMICS OF THE FACE FLY, MUSCA AUTUMNALIS, Elliot S. Krafsur, Roger D. Moon 503

PERITROPHIC MATRIX STRUCTURE AND FUNCTION, M. J. Lehane 525

GENETIC DISSECTION OF SEXUAL BEHAVIOR IN DROSOPHILA MELANOGASTER, Daisuke Yamamoto, Jean-Marc Jallon, Akira Komatsu 551

BIOLOGY OF WOLBACHIA, John H. Werren 587

BIOLOGICAL MEDIATORS OF INSECT IMMUNITY, Jeremy P. Gillespie and, Michael R. Kanost, Tina Trenczek 611

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BEHAVIORAL MANIPULATION METHODS FOR INSECT PEST

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