**3. Mating disruption**

The acceptance of the communication-disruption tactic has largely been driven by dissat‐ isfaction with the control levels achieved with conventional insecticides, often because of emerging resistance problems. Furthermore, in contrast to insecticides, the effectiveness of mating disruption increases with long-term use, resulting in a substantial reduction of populations.

Most of the studies on the use of attractants to disrupt a finding behavior have focused on mate location, particularly of moths, in the so-called mating disruption method. This control method has come to prominence in pest control the last decades. Its success has been observed in controlling several pests like the pink bollworrn, *Pectinophora gossypiella* on cotton; the oriental fruit moth, *Grapholita molesta*, on stone fruits; tomato borer fruit *Neoleucinodes elegantalis*, in tomato and codling moth, *Cydia pomonella* in apple, in which codling moth mating disruption enables sustainable and reliable control at low population densities.

This method consists of distributing a large amount of synthetic sex pheromone in the field, aiming to prevent the male to find a female, disrupting mating. Therefore, new pest genera‐ tions do not occur on treated area. Nevertheless the success of this method is associated with pest migratory ability and biological aspects. According to reference (Cardé & Minks 1995) the use of sexual disruption certainly results in success, due to its ability to reduce the local population of the pest. However, it does not protect the area of immigration from outside populations, when used in an isolated way by a single producer or when there is no geographic isolation (geographic barriers). In order to avoid these potential problems, to ensure that this method will obtains the desirable success, it is required a good knowledge about the ecology of the pest and its immigration ability, aiming the entry capacity of mated females, coming from outside the treated area. The sphere of lures influence must be determinate for obtaining the distance between them in the field. Research will focus on determining the number of lures, their dosages and their spatial arrangement to reduce mating success.

The logistics involved in implementing the method, also deserves attention, as it requires an accurate monitoring program, based on samplings with traps baited with pheromone, to determine or even to ensure that the use of disruption is enough to keep the pest population levels under the economic threshold level, thus justifying the method.

#### **3.1. Mating disruption mechanisms**

densities, be easy to handle and to carry and also should have low cost, high durability and strength. These parameters, which should be determined, are essential for successful moni‐

The monitoring has been used on many economic important pest worldwide using traps containing pheromone to estimate population density in important crops such as maize and tomato. The reports of its use to estimate populations of *Spodoptera frugiperda* (Mitch‐ ell *et al*. 1985, Tumlinson *et al.* 1986), *Ostrinia nubilalis* (Hudon *et al.* 1989), *Keiferia lycoper‐ sicella* (Ridgway *et al*. 1990) and *Tuta absoluta* (Charlton *et al.* 1991) shows that this is not a new tool of pest management. However, given the current need for sustainability of agri‐ cultural activities, such monitoring proved to be economically viable and environmentally sustainable, by determining the ideal time of interventions to reduce the population of

Besides pheromone use, monitoring can be performed based on visual stimuli. Insects that use vision to locate hosts can be monitored with the aid of colored traps. The princi‐ ple of this method is to ensure that the insects are lured into a colored surface impregnat‐ ed with glue. In reference (Natwick *et al.* 2007) it was recorded the efficacy of colored sticky traps to detect and monitor *Frankliniella occidentalis* in lettuce. In this particular case, the blue color would be more suitable. Studies have indicated that while there are no insects caught in traps, there is no need to carry out chemical control. The adoption of this monitoring by lettuce growers can reduce insecticide applications in the field. It should be noted that when using visual stimuli, based on color as attractant in traps, the

Food attractants can also be used for monitoring pests. In horticulture, the technique is widely used to monitor fruit flies. In this case, food baits are used in traps to attract in‐ sects. Several attractants, such as brown sugar, sucrose, hydrolyzed corn protein, fruit juice and wine vinegar in McPhail, Jackson and PET bottles traps are used for monitor‐ ing (Nascimento *et al.* 2000). One example is the use of orange and grape juices at a con‐ centration of 25% that are being used in monitoring *Anastrepha fraterculus* in peach

The acceptance of the communication-disruption tactic has largely been driven by dissat‐ isfaction with the control levels achieved with conventional insecticides, often because of emerging resistance problems. Furthermore, in contrast to insecticides, the effectiveness of mating disruption increases with long-term use, resulting in a substantial reduction of

Most of the studies on the use of attractants to disrupt a finding behavior have focused on mate location, particularly of moths, in the so-called mating disruption method. This control method has come to prominence in pest control the last decades. Its success has been observed in

toring.

pests in the field.

preference of the target insect must be followed.

178 Insecticides - Development of Safer and More Effective Technologies

orchards (Guerra *et al.* 2007).

**3. Mating disruption**

populations.

The sex pheromone may act through different mechanisms in mating disruption, however, the main behavioral mechanisms have been defined as sensory fatigue by diminution of response due to sensory adaptation or habituation, arrestment of upwind flight at high concentrations, shifting the rhythm of response to females, changing the fine structure of or camouflaging a natural plume, outcompeting females, and causing an imbalance of sensory inputs by altering the perceived blend. 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 mechanisms used by male moths in response to pheromone, behavioral control has not been widely used in pest man‐ agement (Cardé & Minks 1995, Foster & Harris 1997). In this chapter we discuss some of these mechanisms, as follows.

Diminution in responsiveness via either sensory adaptation or habituation: Encounters with formulated pheromone may raise the males response threshold or abolish responsiveness entirely. Either outcome could result from adaptation of peripheral receptors on the antennae or habituation at a central processing level. Continuous release of pheromone formulation, leading to its constant presence in the area, increases habituation.

Shifting the rhythm of response: The continuous presence of pheromone can cause males to respond to formulated pheromone well before females call. Such precocious male activity could contribute to a diminished response when females commence pheromone release.

Camouflage of the plumes from calling females: At some distance downwind of a moth releasing pheromone, the concentration of pheromone emitted from the moth's odor plume should be rendered imperceptible in a background of synthetic pheromone. At those distances the male would be unable to distinguish the natural plume filaments.

Competition between calling females and point sources of synthetic pheromone: Males may remain responsive and orient to pheromone plumes from point-source release devices. The ratio of dispensers to calling females and their comparative attractiveness will set the intensity of competition. The time spent orienting to artificial point sources of pheromone lessens the time available to orient to plumes from calling females.

#### **3.2. Dispenser technology**

Practical applications of the mating disruption technique require efficient and economic dispenser materials that release sufficient amounts of pheromone over an extended period. The pheromone dispenser technology determines the efficacy and the economics of mating disruption.

The importance of adequate rate release and consistently for long periods is undisputed in this technique success. That can be observed by several studies testing different release technolo‐ gies (dispensers), as observed in references (Knight *et al.* 2012) and (Bohnenblust *et al.* 2012). As some successful technologies, we mention the sealed polyethylene vials and the SPLAT®- Specialized Pheromone & Lure Aplplication Technology (Figure 1).

Sealed polyethylene vials with pheromone kept the communication disruption for the millet stem borer, *Coniesta ignefusalus* for up to three months in millet farmers' fields (Youm *et al.* 2012). SPLAT emitters, which is an emulsion paste (wax) and amorphous that controls the release of insecticides and semiochemical was effective to achieve communication disruption by season-long for several Lepidoptera pests like *N. elegantalis* in tomato (França et al. in 2012, unpublished data), *Bonagota salubricola* and *G. molesta* in peach (Härter *et al.* 2010, Stelinski *et al.* 2010) and *Phyllocnistis citrella* in citrus (Stelinski *et al.* 2007).

**Figure 1.** SPLAT NEO (containing *Neoleucinodes elegantalis* pheromone) on tomato crop in Bezerros, PE. At the top

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181

Others technologies have also been used as the microencapsulated formulation. A fort‐ nightly application of the sex pheromone using this technology in peach orchards pre‐ vented the chemical communication between the male and female of *G. molesta*, reducing male catch in traps baited with commercial pheromone. Thus, both the SPLAT® and the microencapsulated pheromone was effective to interrupt the chemical communication of *G. molesta* in peach orchards, even when this was associated with *B. solubricola* phero‐

An important point is that in several management programs disruptants may need to be used in combination with conventional insecticides, the latter either to reduce initial populations or as an adjuvant to the disruptant. In these cases, a reduction in the use of conventional insec‐ ticides is an additional consideration in assessing whether a disruption program is successful (Cardé & Minks 1995). The use of synthetic insecticides associated with pheromone in order to increase the efficiency of control in some situations (Witzgall *et al*. 2008) could increase the

**3.3. Association of mating disruption with synthetic insecticides**

left, the applicator used.

mone (Botton *et al.* 2005).

adoption of this control technique.

Not only the pheromone dispenser technology, but the amount of dispensers is an im‐ portant factor for the efficiency of male mating disruption, since it influences the mecha‐ nisms involved in this process. The number of pheromone release sites is related to the initial density of the pest, for when the density is high the number of dispensers has to be raised, in order to obtain the effectiveness of the method. Härter *et al.* (2010) achieved an efficient control of *G. molesta* in peach, using 1000 release sites (with SPLAT® technol‐ ogy) of pheromone, reducing male catch and the damage from this pest. Pastori et al. (2008) testing 1000 release sites (SPLAT® technology) of *B. salubricola* pheromone associat‐ ed with *G. molesta* pheromone in apple, reduced male catch in both species in the first season. In the following season the catch reduction was only observed for *G. molesta*, however, it did not reflect in damage reduction. For the millet stem borer, *C. ignefusalus* suppression of male catch was obtained when the crops were treated with 400 dispens‐ ers / ha (Youm *et al.* 2012).

Camouflage of the plumes from calling females: At some distance downwind of a moth releasing pheromone, the concentration of pheromone emitted from the moth's odor plume should be rendered imperceptible in a background of synthetic pheromone. At those distances

Competition between calling females and point sources of synthetic pheromone: Males may remain responsive and orient to pheromone plumes from point-source release devices. The ratio of dispensers to calling females and their comparative attractiveness will set the intensity of competition. The time spent orienting to artificial point sources of pheromone lessens the

Practical applications of the mating disruption technique require efficient and economic dispenser materials that release sufficient amounts of pheromone over an extended period. The pheromone dispenser technology determines the efficacy and the economics of mating

The importance of adequate rate release and consistently for long periods is undisputed in this technique success. That can be observed by several studies testing different release technolo‐ gies (dispensers), as observed in references (Knight *et al.* 2012) and (Bohnenblust *et al.* 2012). As some successful technologies, we mention the sealed polyethylene vials and the SPLAT®-

Sealed polyethylene vials with pheromone kept the communication disruption for the millet stem borer, *Coniesta ignefusalus* for up to three months in millet farmers' fields (Youm *et al.* 2012). SPLAT emitters, which is an emulsion paste (wax) and amorphous that controls the release of insecticides and semiochemical was effective to achieve communication disruption by season-long for several Lepidoptera pests like *N. elegantalis* in tomato (França et al. in 2012, unpublished data), *Bonagota salubricola* and *G. molesta* in peach (Härter *et al.* 2010, Stelinski

Not only the pheromone dispenser technology, but the amount of dispensers is an im‐ portant factor for the efficiency of male mating disruption, since it influences the mecha‐ nisms involved in this process. The number of pheromone release sites is related to the initial density of the pest, for when the density is high the number of dispensers has to be raised, in order to obtain the effectiveness of the method. Härter *et al.* (2010) achieved an efficient control of *G. molesta* in peach, using 1000 release sites (with SPLAT® technol‐ ogy) of pheromone, reducing male catch and the damage from this pest. Pastori et al. (2008) testing 1000 release sites (SPLAT® technology) of *B. salubricola* pheromone associat‐ ed with *G. molesta* pheromone in apple, reduced male catch in both species in the first season. In the following season the catch reduction was only observed for *G. molesta*, however, it did not reflect in damage reduction. For the millet stem borer, *C. ignefusalus* suppression of male catch was obtained when the crops were treated with 400 dispens‐

the male would be unable to distinguish the natural plume filaments.

Specialized Pheromone & Lure Aplplication Technology (Figure 1).

*et al.* 2010) and *Phyllocnistis citrella* in citrus (Stelinski *et al.* 2007).

time available to orient to plumes from calling females.

180 Insecticides - Development of Safer and More Effective Technologies

**3.2. Dispenser technology**

ers / ha (Youm *et al.* 2012).

disruption.

**Figure 1.** SPLAT NEO (containing *Neoleucinodes elegantalis* pheromone) on tomato crop in Bezerros, PE. At the top left, the applicator used.

Others technologies have also been used as the microencapsulated formulation. A fort‐ nightly application of the sex pheromone using this technology in peach orchards pre‐ vented the chemical communication between the male and female of *G. molesta*, reducing male catch in traps baited with commercial pheromone. Thus, both the SPLAT® and the microencapsulated pheromone was effective to interrupt the chemical communication of *G. molesta* in peach orchards, even when this was associated with *B. solubricola* phero‐ mone (Botton *et al.* 2005).

#### **3.3. Association of mating disruption with synthetic insecticides**

An important point is that in several management programs disruptants may need to be used in combination with conventional insecticides, the latter either to reduce initial populations or as an adjuvant to the disruptant. In these cases, a reduction in the use of conventional insec‐ ticides is an additional consideration in assessing whether a disruption program is successful (Cardé & Minks 1995). The use of synthetic insecticides associated with pheromone in order to increase the efficiency of control in some situations (Witzgall *et al*. 2008) could increase the adoption of this control technique.

Often the use of this technique reduces the male catch, causing mating disruption, however it does not imply reducing the damage caused by the pest. Probably, this should occur by the en‐ try of mated females originating from untreated areas, so specific applications of insecticides may be indicated to reduce this negative effect. Although, Pastori *et al.* (2008) reported that us‐ ing SPLAT® dispensers containing *B. salubricola* pheromone associated with *G. molesta* phero‐ mone, with or without cypermethrin in the formulation, found that the presence of the insecticide did not affect the results. Moreover, França et al. (2012) (unpublished data) ob‐ tained a greater reduction in both male catch of *N. elegantalis,* oviposition on fruits and damage reduction, when used SPLAT® dispensers containing pheromone associated with cypermeth‐ rin compared with SPLAT® containing only pheromone (Figure 2). The mating disruption tech‐ nique led to the same reduction of damage caused by *G. molesta* in peach orchards, compared with orchards submitted to insecticide spraying, demonstrating the great advantage of using this method (Härter *et al.* 2010). Therefore, using mating disruption, the number of insecticide applications can be reduced or even absence, making the production environmentally sustain‐ able and economically viable, since the money spent on insecticides can be used in obtaining the product to carry out the disruption. Thus, this tactic is quite appropriate for cultures where no residues of pesticides is required or desired, such as fruits for export; and with the consumer profile in transition, becoming increasingly discerning, the search for an alternative control method is essential to the acceptance and retention of the farmer in the current scenario.

**4. Attract-and-kill (A&K) System**

upon contact, kills the insect.

plants and food.

tems.

the stability and longevity of the system.

A novel approach using sex pheromones is the attract-and-kill system. This strategy is a new pest management technique, an extension of mating disruption, which is character‐ ized by the inclusion of an insecticide (killing agent) in addition to the pheromone active ingredient or a feeding attractant (attracting agent). By doing this, it is possible to ach‐ ieve the same control methods as mating disruption, with the potential for increased effi‐ cacy, resulting from the toxicity of the insecticide (Ebbinghaus *et al.* 2001). Unlike mating disruption, which functions by "confusing" the insect, attract-and-kill system attracts the insect to a pesticide laden gel matrix, distributed as small droplets in the crop, which,

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With this system, blanket coverage of the crop is not necessary, and so the amount of insecticide can be significantly reduced. Such an approach would permit reductions in the amounts of insecticides used and would minimize contact with the environment, the crop, and beneficial organisms. An additional benefit of an attract-and-kill formulation is that these formulations generally require less pheromone to be effective, since the target species does not need to be

However, when pheromones are used as the attracting agent, only males are killed. Never‐ theless, removal of males from a population may not have a significant effect on reproduction unless a large percentage of the male population is killed, as a small percentage of the male population will serve to mate with most sexually receptive females. Thus, the development of an attract-and-kill system might be enhanced with chemical lures that are effective in bringing females into a target. Although the majority of chemical attractants are female-produced sex attractants that lure males, female may use chemical odorants to locate and select mates, host

The use of attract-and-kill suffers from some of the same constraints as mating disruption, including the high degree of pest selectivity, a reduction in efficacy with increasing pest density and risk of immigration of mated females. Besides, the different longevity in the insecticide activity and the attractiveness of the droplets set a time-limit for the application. The attractand-kill drops often deteriorated quite rapidly under some weather conditions, such as powerful storms, pelting rain, intense heat, and solar radiation. These conditions may affect

As with any management tool, the operational use of pheromones must be considered within the context of an integrated pest management system. Commercialization of the attract-andkill approach has been undertaken by IPM Technologies Inc., who has global rights to a proprietary and patented matrix, combining insecticide and attractant in a UV sensitive carrier material. Marketed as "Sirene ™" and "Last-Call™ " in Europe and the U.S., respectively, this technology was granted US EPA registration in 1998 and California registration in 1999. The robust matrix can accept, protect and release a wide variety of chemicals (acetates, alcohols, aldehydes) so it has the potential to be deployed against many pest species in diverse ecosys‐

overwhelmed by the pheromone; it only needs to be attracted to it.

**Figure 2.** Mean number of *N. elegantalis* eggs throughout tomato crop cycle, variety TY, treated with Splat 1 (with cypermethrin), Splat 2 (without cypermethrin) and control (led by the producer) submitted to treatments 20 and 30 days after transplanting (Camocim de São Félix, Pernambuco, Brazil, 2011-2012). Columns with different letters are significantly different (p>0.05) by Tukey test.
