**3. Biological influences on pest status**

Although *L. sativae* was the predominant leafminer pest in California during the middle of the 20th century, it was not considered to be a major pest (Parrella, 1982; Trumble, 1981). Sporadic outbreaks of the species now recognized as *L. langei* did occur through coastal areas of California during the 1930s - 1950s (Elmore & Ranney, 1954; Frick, 1951; 1957; 1958; Lange, 1949; Lange et al., 1957). These outbreaks tended to be relatively short lived events, with *L. langei* reverting to a minor pest in between outbreaks. However, beginning in the mid 1990s sustained pest problems with *L. langei* emerged in coastal California (Heinz &

*Liriomyza huidobrensis* was not widely discussed as an important pest in South America until the 1970s (Chavez & Raman, 1987). The change in its pest status at that time has been attrib‐ uted to insecticide induced outbreaks that resulted from intense insecticide treatments made against the primary pest of potato (*Solanum tuberosum* L.) in Peru, the leafmining moth *Tuta absoluta* (Meyrick) (Lepidoptera: Gelechiidae). According to this hypothesis, constant expo‐ sure to insecticides for *T. absoluta* led to the evolution of resistance in *L. huidobrensis* popula‐ tions, but the parasitoids that had contained *L. huidobrensis* populations were eliminated, creating classic secondary pest outbreaks (Luck et al., 1977). As a conclusion, the emergence of *Liriomyza* spp. as consistently important pests can be attributed to the selection for insecti‐

In the mid 1970s, as more frequent and severe outbreaks of *Liriomyza* spp. began to be observed (e.g., Chavez & Raman, 1987; Leibee & Capinera, 1995; Oatman & Kennedy, 1976), leafminers began to emerge as globally important invasive pests of a wide range of horticultural crops. At this time, international trade in horticultural products (e.g., fruits, vegetables and cut flowers) began to escalate tremendously (Huang, 2004), which provided the opportunity for *Liriomyza* spp. to spread through the world on infested

Invasions of these *Liriomyza* spp. has continued unabated from the 1970s through to the present (Abe & Kawahara, 2001; Lei et al., 1997; Scheffer et al., 2006; Weintraub & Horowitz, 1995). All three of the major pest species now occur on all continents, except Antarctica. Even though the three major pest species share the common characteristic of being trans‐ ported to new geographic areas via exported plant material, they have their own unique in‐ vasion histories. In many regions, more than one of the species has been introduced. These sympatric introductions have led to many complex interactions among the species, whereby

The introduction of *L. trifolii* into California, beginning in the late 1970s from plant mate‐ rial shipped from Florida brought the issue of invasive leafminers to the fore (Parrella, 1987). Soon after its introduction into California, *L. trifolii* displaced the previously estab‐ lished *L. sativae* as the predominant species in the state (Trumble & Nakakihara, 1983). To a large degree, this displacement appears to have resulted from the lower susceptibil‐ ity of *L. trifolii* to commonly used insecticides (Palumbo et al., 1994; Reitz & Trumble, 2002a). The establishment of *L. trifolii* in California facilitated its spread to other coun‐ tries, as infested propagation plants are shipped to production facilities in other coun‐ tries. Then, final products are redistributed from these countries to yet other countries

one species is able to displace another previously established invasive species.

Chaney, 1995; Reitz et al., 1999).

236 Insecticides - Development of Safer and More Effective Technologies

cide resistant populations.

plant material (Minkenberg, 1988a).

The pest status of *Liriomyza* spp. is closely tied to their biology. In part, their pest status re‐ sults from the ability of populations of these flies to build up rapidly. Although there is con‐ siderably variation in the fecundity of *Liriomyza* spp. across studies, it is clear that females have a high reproductive capacity. For example, the mean fecundity for *L. sativae* females observed by Tokumaru and Abe (2003) was over 600 eggs per female. Although this may be an unusual observation, other studies routinely report fecundity in excess of 100 eggs per female. These species also have very rapid developmental rates, with a generation able to be completed in fewer than 20 days at optimal temperatures (Lanzoni et al., 2002; Minkenberg, 1988b; Parkman et al., 1989). Consequently, multiple, overlapping generations can be pro‐ duced within a single cropping season. *Liriomyza sativae, L. trifolii* and *L. huidobrensis* are among the few members of the genus that are highly polyphagous. The host range of each species encompasses hundreds of species in a wide range of plant families (Spencer, 1990). This polyphagy allows populations of these species to develop on multiple crops, as well as uncultivated hosts, and then disperse into newly planted crops (Jones & Parrella, 1986; Trumble & Nakakihara, 1983; Tryon et al., 1980). Their polyphagy also presents many op‐ 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).

conditions. Since that time, both have been commercially available. Despite this long history of use, resistance has not been a major problem in their use (Ferguson, 2004). The one re‐ corded case of resistance to cyromazine cited in that study showed that reversion to suscept‐ ibility occurred within 8 generations in a laboratory strain and that field efficacy was

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

http://dx.doi.org/10.5772/53874

239

Another class of insecticide with efficacy against *Liriomyza* spp. is the spinosyn class (spino‐ sad and spinetoram). Spinosyn insecticides have been widely used since their introduction in the US in 1997. Similar to abamectin and cyromazine, spinosyns have translaminar prop‐ erties, enabling them to target leafminer larvae. Spinosyns are neurotoxins also. However, they have a different mode of action than abamectin, one that disrupts nicotinic acetylcho‐ line receptors (Salgado, 1998). Spinosyns are classified as Group 5 insecticides and abamec‐ tin is classified as a Group 6 insecticide by the Insecticide Resistance Action Committee (IRAC International MoA Working Group, 2011). There have been few reports of resistance to spinosyns to date among *Liriomyza* spp. (Ferguson, 2004). The lack of reported cases of spinosyn resistance may be considered surprising, given that spinosyn products are widely used against other key pests that co-occur with leafminers, including thrips and Lepidoptera pests (Demirozera et al., 2012; Reitz & Funderburk, 2012; Reitz et al., 1999). Incorporating the use of a penetrating surfactant improves the efficacy of spinosad against *Liriomyza* larvae (Bueno et al., 2007), allowing growers to improve management with lower rates of insecti‐ cide. This approach may also help reduce selection pressures. It is reasonable that increasing penetration of abamectin or cyromazine into plants would, likewise, increase their efficacy.

Selection of appropriate insecticides and rates for use in the field also depends upon proper identification of leafminer species. Parrella and Keil (1985) found that *L. trifolii* was much less susceptible to methamidophos than was *L. sativae* or *L. langei.* Likewise, *L. trifolii* populations in China are significantly less susceptible to abamectin and cyroma‐ zine than are populations of *L. sativae* (Gao et al., 2012) In contrast in Japan, *L. sativae* populations were less susceptible to several commonly used insecticides than were local populations of *L. trifolii* (Tokumaru et al., 2005). There is evidence that invasive popula‐ tions of *L. huidobrensis* are more tolerant to certain commonly used insecticides than are

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‐

restored within 2 seasons of reduced exposure.

sympatric populations of *L. trifolii* (Weintraub, 2001a).

cides with low toxicity to *Liriomyza* parasitoids (e.g., Wene, 1953).

**5. Management trends**
