**5. Management trends**

portunities for movement on plant material to new regions. As the eggs and larvae of *Lirio‐ myza* spp. are concealed internally within plant foliage, they can be easily moved within shipments from production areas to final markets, and detection is difficult (Parrella, 1987).

One of the most important factors in leading to *Liriomyza* spp. becoming pests is their ability to evolve resistance to insecticides (Parrella & Keil, 1984). Leibee (1981) compiled a list of insecticides used against *Liriomyza* spp. in Florida and the life spans of their field efficacy in commercial use. The list of ineffective materials includes almost all classes of insecticides de‐ veloped up to that time. Some insecticides became ineffective in as little as two years. This review confirmed the widespread importance of insecticide resistance in driving the pest status of *Liriomyza* spp. Despite the rapid failures of different insecticides, there has been a general belief, at least through the middle of the 20th century, that new chemistries would become available to replace ineffective ones, and provide a few additional seasons of con‐ trol. Consequently, there was little emphasis on alternative management techniques until

the advent of the worldwide leafminer crisis in the 1970s (Leibee & Capinera, 1995).

maintained their resistance for 5 years, or that carbamates are not toxic to *L. trifolii.*

At present, two of the most effective insecticides for *Liriomyza* management are abamectin and cyromazine. Both insecticides target the larvae inside the plant foliage. Cyromazine acts as a growth regulator; whereas abamectin is a neurotoxin that acts as a GABA agonist. Both have translaminar properties, allowing them to reach the larvae within the plant. Research by Schuster and Everett (1983) documented the effectiveness of both insecticides under field

& Keil, 1985), eradication programs may not be successful.

Intense insecticide use is the most common strategy used to eradicate newly discovered out‐ breaks of *Liriomyza* spp. (Bartlett & Powell, 1981). The success of this strategy is dependent on the susceptibility of invasive populations to available insecticides. Because invasive pop‐ ulations are already likely to be resistant to various insecticides (MacDonald, 1991; Parrella

Cross resistance to multiple classes of insecticides is also likely in *Liriomyza* spp. Despite a short history of pyrethroid use in Hawaii, high levels of tolerance to fenvalerate and perme‐ thrin were detected in field populations of both *L. sativae* and *L. trifolii* (Mason et al., 1987). The authors speculated that the tolerance/resistance arose as a result of cross-resistance to longer used organochlorine insecticides, which have a similar mode of action to pyrethroids. Populations of invasive *L. trifolii* obtained from greenhouses in Canada treated intensively with the organophosphate pyrazophos for less than 1 year showed high levels of resistance to that insecticide and to other types of organophosphates that had not been used previous‐ ly (Broadbent & Pree, 1989). Fortunately from a pest management perspective, reversion to susceptibility to organophosphates and pyrethroids has been shown to occur within a few generations (within 1 year) (Broadbent & Pree, 1989; Parrella & Trumble, 1989). Interesting‐ ly, these Canadian populations showed no susceptibility to carbamates. It is possible that these populations were already resistant to carbamates and that laboratory-reared flies

**4. Response to insecticides**

238 Insecticides - Development of Safer and More Effective Technologies

The premise that leafminers are secondary pests, which are released from natural control when their enemies are eliminated (Luckmann & Metcalf, 1994), has a long history, even if it has not always been fully appreciated. Studies dating back to the 1940s have shown the im‐ portance of parasitoids in maintaining *Liriomyza* spp. populations below economically dam‐ aging levels (Hills & Taylor, 1951) and where parasitoid populations are reduced in agroecosystems, there are outbreaks of *Liriomyza* spp. populations (Oatman & Kennedy, 1976; Ohno et al., 1999). Consequently, there has long been interest in identifying insecti‐ cides with low toxicity to *Liriomyza* parasitoids (e.g., Wene, 1953).

In every geographic region where *L. huidobrensis, L. sativae* or *L. trifolii* are indigenous, there is a rich complex of hymenopteran parasitoids (Liu et al., 2009). Parasitoid complexes associ‐ ated with *Liriomyza* spp. generally consist of several species of larval and larval-pupal hyme‐ nopteran parasitoids. Many, but not all, of the species are oligophagous so that they may attack the different pest species and native non-pest *Liriomyza* spp. (Nicoli, 1997)*.* It should be noted that there is evidence of differential parasitism across *Liriomyza* spp. Although, many parasitoids of *Liriomyza* are fairly generalized and are able to successfully attack vari‐ ous species, their reproductive success varies with the host (Abe et al., 2005) Still other para‐ sitoids are not able to parasitize all *Liriomyza* species. This differential parasitism ability can have extreme implications for leafminer ecology. Greater levels of parasitism of *L. trifolii* than of *L. sativae* has been cited as one of the key factors in the displacement of *L. trifolii* by *L. sativae* in Japan (Abe et al., 2005; Abe & Tokumaru, 2008).

Of the three most effective insecticides for use against *Liriomyza* spp. today (abamectin, cyromazine, spinosyns), there have been variable conclusions regarding their effects on *Liriomyza* spp. parasitoids. Cyromazine is the least detrimental of these insecticides to *Liriomyza* parasitoids. As a growth regulator specific to Diptera, it does not directly affect the development of parasitic Hymenoptera. It does reduce the number of available hosts, and it will kill *Liriomyza* larvae before parasitoids may complete their development. However, these effects should complement the action of parasitoids to enhance overall

Insecticide Use and the Ecology of Invasive *Liriomyza* Leafminer Management

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241

Results of various studies provide conflicting results for the effect of abamectin on leaf‐ miner parasitoids (reviewed in Kaspi & Parrella, 2005). In general, field studies have demonstrated that abamectin and spinosyns are not as detrimental to parasitoid popula‐ tions as carbamates, organophosphate or pyrethroids, but they are more deleterious than cyromazine (Prijono et al., 2004; Schuster, 1994; Trumble, 1985). The greater toxicity of abamectin and spinosyns compared with cyromazine to *Liriomyza* spp. parasitoids have been demonstrated in laboratory studies (Babul Hossain & Poehling, 2006; Bjorksten & Robinson, 2005). In particular, abamectin and spinosyns are lethal to parasitoid adults. Interestingly, parasitoid populations may rebound faster in abamectin treated fields com‐ pared with cyromazine treated fields, a result attributed to the longer residual period of cyromazine (Weintraub, 2001b). These results clearly show that insecticide use should be approached cautiously and that growers should be encouraged to consider the costs and

In recognition of the importance that parasitoids play in managing leafminers, Trumble and colleagues initiated development of IPM programs for field grown vegetables in California and Mexico. One of the first aspects addressed in the research program was to establish real‐ istic economic thresholds in these agroecosystems for the key insect pests, *L. trifolii* and the beet armyworm, *Spodoptera exigua* (Hübner) (Lepidoptera: Noctuidae) (Reitz et al., 1999; Trumble, 1985; Trumble & Alvarado-Rodriguez, 1993; Trumble et al., 1997). According to program guidelines, when systematic sampling shows pest populations exceeding economic thresholds, growers would select an insecticide to bring the populations under damaging levels. The key to maintaining stable management of *Liriomyza* spp. rests in selecting insecti‐

In commercial scale trials conducted in celery (*Apium graveolens* L.) and tomato, these IPM programs were compared with conventional high input management programs. In‐ secticides for the IPM programs consisted of *Bacillus thuringiensis,* tebufenozide (an insect growth regulator) and spinosad for management of Lepidoptera, and abamectin and cy‐ romazine for *Liriomyza* management (Reitz et al., 1999; Trumble & Alvarado-Rodriguez, 1993; Trumble et al., 1997). To minimize the risk of insecticide resistance, growers are en‐ couraged to rotate abamectin and cyromazine, should multiple applications be needed in a crop. The conventional, high input management programs reflected standard grower practices of the time and included weekly applications of broad spectrum synthetic insec‐ ticides, including methomyl (carbamate), permethrin (pyrethroid) and methamidophos

cides that are the least disruptive to the leafminer parasitoid complex.

management of *Liriomyza* pests.

benefits of different insecticide uses.

(organophosphate).

Parasitoids associated with native non-pest *Liriomyza* spp. have the potential to provide bio‐ logical control of invasive leafminers because the native hosts serve as reservoirs for parasi‐ toids populations (Chen et al., 2003; Nicoli, 1997; Tran et al., 2006) Often, parasitoids of *Liriomyza* pest species are introduced along with their alien hosts (Bjorksten et al., 2005; Ta‐ gami et al., 2006). These relationships may then be exploited as a form of unintended classi‐ cal biological control.

Whereas parasitoids are valuable control agents, making effective use of them in practice can be challenging. Parasitoid populations, by their nature, will lag behind the develop‐ ment of their host populations (Hofsvang et al., 2005; Trumble & Nakakihara, 1983; Weintraub, 2001a). In these types of situations, growers may need to apply insecticides to keep growing leafminer populations below economically damaging levels. In a similar vein, growers may need to use insecticides to treat other pest problems, which then may have detrimental effects on leafminer management (Getzin, 1960). The outcome of either situation is that leafminer populations are released from their natural control and rapidly increase because many of the insecticides used against leafminers or other pests are high‐ ly toxic to their parasitoids. Should such a rapid increase occur growers are likely to be‐ lieve that further insecticide treatments are warranted. This then becomes the very definition of the pesticide treadmill.

Most broad spectrum synthetic insecticides developed since the 1940s are highly toxic to parasitoids of *Liriomyza* spp. (Hidrayani et al., 2005; Oatman & Kennedy, 1976; Saito et al., 1996; Schuster, 1994). Classes of insecticides that have shown high toxicity to parasitoids in‐ clude carbamates, organochlorines, organophosphates and pyrethroids, which are also in‐ secticides that show limited efficacy against *Liriomyza* spp. (Hara, 1986; Hidrayani et al., 2005). Therefore, these types of insecticides should be used with great caution in systems where *Liriomyza* spp. are key pests. Several studies have shown that parasitoids are able to evolve resistance to insecticides under routine selection pressures in the field (Rathman et al., 1990; Spollen et al., 1995). Should parasitoids be resistant to a particular insecticide, that insecticide could be integrated into (IPM) programs. This would be especially true if the in‐ secticide were targeting another pest species. However, to be effective, levels of resistance in the parasitoid population must exceed the field rate of the insecticide.

Of the three most effective insecticides for use against *Liriomyza* spp. today (abamectin, cyromazine, spinosyns), there have been variable conclusions regarding their effects on *Liriomyza* spp. parasitoids. Cyromazine is the least detrimental of these insecticides to *Liriomyza* parasitoids. As a growth regulator specific to Diptera, it does not directly affect the development of parasitic Hymenoptera. It does reduce the number of available hosts, and it will kill *Liriomyza* larvae before parasitoids may complete their development. However, these effects should complement the action of parasitoids to enhance overall management of *Liriomyza* pests.

In every geographic region where *L. huidobrensis, L. sativae* or *L. trifolii* are indigenous, there is a rich complex of hymenopteran parasitoids (Liu et al., 2009). Parasitoid complexes associ‐ ated with *Liriomyza* spp. generally consist of several species of larval and larval-pupal hyme‐ nopteran parasitoids. Many, but not all, of the species are oligophagous so that they may attack the different pest species and native non-pest *Liriomyza* spp. (Nicoli, 1997)*.* It should be noted that there is evidence of differential parasitism across *Liriomyza* spp. Although, many parasitoids of *Liriomyza* are fairly generalized and are able to successfully attack vari‐ ous species, their reproductive success varies with the host (Abe et al., 2005) Still other para‐ sitoids are not able to parasitize all *Liriomyza* species. This differential parasitism ability can have extreme implications for leafminer ecology. Greater levels of parasitism of *L. trifolii* than of *L. sativae* has been cited as one of the key factors in the displacement of *L. trifolii* by *L.*

Parasitoids associated with native non-pest *Liriomyza* spp. have the potential to provide bio‐ logical control of invasive leafminers because the native hosts serve as reservoirs for parasi‐ toids populations (Chen et al., 2003; Nicoli, 1997; Tran et al., 2006) Often, parasitoids of *Liriomyza* pest species are introduced along with their alien hosts (Bjorksten et al., 2005; Ta‐ gami et al., 2006). These relationships may then be exploited as a form of unintended classi‐

Whereas parasitoids are valuable control agents, making effective use of them in practice can be challenging. Parasitoid populations, by their nature, will lag behind the develop‐ ment of their host populations (Hofsvang et al., 2005; Trumble & Nakakihara, 1983; Weintraub, 2001a). In these types of situations, growers may need to apply insecticides to keep growing leafminer populations below economically damaging levels. In a similar vein, growers may need to use insecticides to treat other pest problems, which then may have detrimental effects on leafminer management (Getzin, 1960). The outcome of either situation is that leafminer populations are released from their natural control and rapidly increase because many of the insecticides used against leafminers or other pests are high‐ ly toxic to their parasitoids. Should such a rapid increase occur growers are likely to be‐ lieve that further insecticide treatments are warranted. This then becomes the very

Most broad spectrum synthetic insecticides developed since the 1940s are highly toxic to parasitoids of *Liriomyza* spp. (Hidrayani et al., 2005; Oatman & Kennedy, 1976; Saito et al., 1996; Schuster, 1994). Classes of insecticides that have shown high toxicity to parasitoids in‐ clude carbamates, organochlorines, organophosphates and pyrethroids, which are also in‐ secticides that show limited efficacy against *Liriomyza* spp. (Hara, 1986; Hidrayani et al., 2005). Therefore, these types of insecticides should be used with great caution in systems where *Liriomyza* spp. are key pests. Several studies have shown that parasitoids are able to evolve resistance to insecticides under routine selection pressures in the field (Rathman et al., 1990; Spollen et al., 1995). Should parasitoids be resistant to a particular insecticide, that insecticide could be integrated into (IPM) programs. This would be especially true if the in‐ secticide were targeting another pest species. However, to be effective, levels of resistance in

the parasitoid population must exceed the field rate of the insecticide.

*sativae* in Japan (Abe et al., 2005; Abe & Tokumaru, 2008).

240 Insecticides - Development of Safer and More Effective Technologies

cal biological control.

definition of the pesticide treadmill.

Results of various studies provide conflicting results for the effect of abamectin on leaf‐ miner parasitoids (reviewed in Kaspi & Parrella, 2005). In general, field studies have demonstrated that abamectin and spinosyns are not as detrimental to parasitoid popula‐ tions as carbamates, organophosphate or pyrethroids, but they are more deleterious than cyromazine (Prijono et al., 2004; Schuster, 1994; Trumble, 1985). The greater toxicity of abamectin and spinosyns compared with cyromazine to *Liriomyza* spp. parasitoids have been demonstrated in laboratory studies (Babul Hossain & Poehling, 2006; Bjorksten & Robinson, 2005). In particular, abamectin and spinosyns are lethal to parasitoid adults. Interestingly, parasitoid populations may rebound faster in abamectin treated fields com‐ pared with cyromazine treated fields, a result attributed to the longer residual period of cyromazine (Weintraub, 2001b). These results clearly show that insecticide use should be approached cautiously and that growers should be encouraged to consider the costs and benefits of different insecticide uses.

In recognition of the importance that parasitoids play in managing leafminers, Trumble and colleagues initiated development of IPM programs for field grown vegetables in California and Mexico. One of the first aspects addressed in the research program was to establish real‐ istic economic thresholds in these agroecosystems for the key insect pests, *L. trifolii* and the beet armyworm, *Spodoptera exigua* (Hübner) (Lepidoptera: Noctuidae) (Reitz et al., 1999; Trumble, 1985; Trumble & Alvarado-Rodriguez, 1993; Trumble et al., 1997). According to program guidelines, when systematic sampling shows pest populations exceeding economic thresholds, growers would select an insecticide to bring the populations under damaging levels. The key to maintaining stable management of *Liriomyza* spp. rests in selecting insecti‐ cides that are the least disruptive to the leafminer parasitoid complex.

In commercial scale trials conducted in celery (*Apium graveolens* L.) and tomato, these IPM programs were compared with conventional high input management programs. In‐ secticides for the IPM programs consisted of *Bacillus thuringiensis,* tebufenozide (an insect growth regulator) and spinosad for management of Lepidoptera, and abamectin and cy‐ romazine for *Liriomyza* management (Reitz et al., 1999; Trumble & Alvarado-Rodriguez, 1993; Trumble et al., 1997). To minimize the risk of insecticide resistance, growers are en‐ couraged to rotate abamectin and cyromazine, should multiple applications be needed in a crop. The conventional, high input management programs reflected standard grower practices of the time and included weekly applications of broad spectrum synthetic insec‐ ticides, including methomyl (carbamate), permethrin (pyrethroid) and methamidophos (organophosphate).

These trials consistently showed that the IPM programs had consistently lower populations of *Liriomyza* spp. than the high input conventional programs. These results were seen be‐ cause the IPM programs were able to conserve the leafminer parasitoids. More importantly for growers, because insecticide applications in the IPM programs were based on scouting results and linked to economic thresholds, fewer insecticide applications were made in the IPM programs than in the conventional programs. By focusing on conservation of leafminer parasitoids, growers can reserve use of the few highly efficacious insecticides for situations where there is a danger of leafminer population outbreaks. Limiting their use to these situa‐ tions mitigates the risk of resistance developing to these insecticides.

aging *Liriomyza* populations, to date, it has not been as economically cost effective as the ju‐ dicious use of insecticides (Chow & Heinz, 2006; Ozawa et al., 2001). These economic

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An ideal insecticide for incorporation into a greenhouse IPM program is one that is pest spe‐ cific and not harmful to biological control agents of that pest, or those of other pests in the system (Kaspi & Parrella, 2005). Although not harmless to parasitoids, the use of abamectin can be successfully integrated with augmentative releases of the parasitoid *Diglyphus isaea* (Walker) for management of *L. trifolii* (Kaspi & Parrella, 2005). They found that the residual period for abamectin was approximately 1 week. By releasing parasitoids after that time, the abamectin would no longer be toxic for the parasitoids. In this manner, an early season ap‐ plication of abamectin could sharply lower *L. trifolii* populations quickly, and released para‐ sitoids could then provide longer term management of *L. trifolii. Diglyphus isaea* larvae paralyze their hosts, and consequently some *D. isaea* larvae would be protected from aba‐ mectin sprays because their hosts would no longer be feeding to ingest the toxin. As with the IPM programs for field grown vegetables discussed above, this integrated management program for greenhouse leafminers presents several advantages for growers. Because re‐ leased parasitoids are self-perpetuating, a single release may substitute for several insecti‐ cide applications. Again, this integrated approach reduces the probability of resistance developing. Also, this approach could reduce inputs for growers without sacrificing crop yield and quality. This integrated management program for *L. trifolii* could be expanded into a more comprehensive program by determining how various insecticides and natural ene‐

Growers around the world have experienced significant problems from *Liriomyza* leafmin‐ ers. They continue to invest considerable resources in the management of these pest flies. Despite the long history of problems with leafminers, many of the lessons that have been learned in one area at one time have, unfortunately, had to be relearned elsewhere. Leafmin‐ ers are classic secondary pests. If the parasitoid complex that attacks leafminers is con‐ served, economic damage from leafminers can be mitigated. Still, there are clearly circumstances where insecticides are needed to suppress leafminer populations below eco‐ nomically damaging levels. In particular, there may be cases where the lag in the increase in parasitoid populations may allow leafminer populations to exceed economic threshold lev‐ els. In such situations, growers should select insecticides that will minimally disrupt the par‐ asitoid complex. First and foremost, though, it is imperative that researchers provide growers with realistic economic action thresholds for different cropping systems so that growers have a clear understanding of when their crop may be at risk. Indeed, insecticide treatments may not always be warranted for seemingly high populations of leafminers. Marketable yield for a crop like tomato may not be lowered until exceedingly high levels of

differences make growers less likely to adopt insecticide alternatives

mies for other pests interact with one another.

leafmines are reached (Levins et al., 1975).

**6. Conclusions**

Despite the lower insecticide use, growers were not sacrificing the amount of crop harvested or its quality. Ultimately, these IPM programs based on economic thresholds with the goal of conserving *Liriomyza* spp. parasitoids enable growers to produce high quality crops at lower cost and with typically greater profit than programs with higher insecticide inputs. By including economic comparisons of management programs, these trials provide growers with an economic rationale to alter their management methods (Reitz et al., 1999).

*Liriomyza* spp. management in protected environments, such as enclosed glasshouse and greenhouse production systems, generally requires greater inputs than for field grown crops. Greenhouses are highly managed environments where growers have extensive control over crop conditions (Shipp et al., 1991). Yet, given the potential value of crops and the high production costs, many growers produce crops year round without periods to sanitize facilities. This continuous production is conducted at optimal temperatures for plant and, consequently, insect development. Therefore, the greenhouse environment is highly conducive to the development of pest populations, but colonization by naturally occurring beneficial organisms is restricted. With the lack of naturally occurring biologi‐ cal control available to most greenhouse systems and the high crop value, growers his‐ torically relied on intensive insecticide use for pest management, and this reliance on insecticides has hindered the development of IPM programs for greenhouse production (Parrella & Jones, 1987). Further complicating adoption of IPM programs in greenhouses are the exceedingly low damage threshold for floriculture and vegetable crops that are grown in protected environments (Yano, 2004).

Despite these constraints, there have been successful demonstrations of integrated manage‐ ment of *Liriomyza* spp. and other pests in greenhouse systems. The initial impetus for devel‐ opment of IPM programs has, not surprisingly, been the development of resistance and failure of insecticides to effectively manage pests. IPM programs for greenhouse systems have been widely adopted in northern and western Europe (van Lenteren, 2000). There, nat‐ ural enemies are commercially available for all major pests, including parasitoids in the gen‐ era of *Dacnusa, Diglyphus* and *Opius* for *Liriomyza* management. These parasitoids can be released augmentatively and become established in greenhouses for long term management of leafminers. Because of the high demand for natural enemies to meet the needs of the large European greenhouse industry, mass produced natural enemies are cost effective for Euro‐ pean growers to use. However, while augmentative biological control with parasitoids in the United States and other non-European countries has been shown to be effective in man‐ aging *Liriomyza* populations, to date, it has not been as economically cost effective as the ju‐ dicious use of insecticides (Chow & Heinz, 2006; Ozawa et al., 2001). These economic differences make growers less likely to adopt insecticide alternatives

An ideal insecticide for incorporation into a greenhouse IPM program is one that is pest spe‐ cific and not harmful to biological control agents of that pest, or those of other pests in the system (Kaspi & Parrella, 2005). Although not harmless to parasitoids, the use of abamectin can be successfully integrated with augmentative releases of the parasitoid *Diglyphus isaea* (Walker) for management of *L. trifolii* (Kaspi & Parrella, 2005). They found that the residual period for abamectin was approximately 1 week. By releasing parasitoids after that time, the abamectin would no longer be toxic for the parasitoids. In this manner, an early season ap‐ plication of abamectin could sharply lower *L. trifolii* populations quickly, and released para‐ sitoids could then provide longer term management of *L. trifolii. Diglyphus isaea* larvae paralyze their hosts, and consequently some *D. isaea* larvae would be protected from aba‐ mectin sprays because their hosts would no longer be feeding to ingest the toxin. As with the IPM programs for field grown vegetables discussed above, this integrated management program for greenhouse leafminers presents several advantages for growers. Because re‐ leased parasitoids are self-perpetuating, a single release may substitute for several insecti‐ cide applications. Again, this integrated approach reduces the probability of resistance developing. Also, this approach could reduce inputs for growers without sacrificing crop yield and quality. This integrated management program for *L. trifolii* could be expanded into a more comprehensive program by determining how various insecticides and natural ene‐ mies for other pests interact with one another.
