**2. Taxonomy, origins and invasiveness**

One of the great challenges in understanding the pest status of *Liriomyza* spp. and effectively managing them has been the uncertainty regarding taxonomy and misidentification of pest species. Agromyzidae species occur throughout the world, and many species are morpho‐ logically similar, making distinctions among species difficult. Minkenberg (1988a) suggests that as a consequence invasive populations of *L. trifolii* became well established in some countries because specimens of early colonizers were misidentified as native species, and so no management programs were adopted. More thorough species determinations were not undertaken until widespread crop losses were reported by growers.

Among the three major pest species, there have been considerable historical problems with their taxonomy and identification. *Liriomyza sativae* was originally described from Argentina by Blanchard (1938) and is thought to be endemic to regions of South and North America (Spencer, 1973). It was recorded as a pest of numerous horticultural crops in southern Florida (USA) by the 1940s. Many early records of *Liriomyza* pests in Florida, USA refer to *Liriomyza pusilla* (Meigen) although the actual species of concern was almost certainly *L. sativae* (Spencer, 1973). *Liriomyza sativae* has probably been present in California, USA since the early 20th century, but it is uncertain if the species that Oatman and Michelbarger termed *Liriomyza pictella* (Thomson) in a series of seminal biological studies (Oatman, 1959; 1960; Oatman & Michelbacher, 1958; 1959) was *L. pictel‐ la*, *L. sativae* or another undescribed sibling species.

holes (Bethke & Parrella, 1985). The stippling patterns left from these punctures degrade the aesthetic value of ornamental plants, and sufficiently high levels of this puncture damage can reduce plant photosynthesis (Trumble et al., 1985). In addition, young seedling plants can be killed by intense puncture damage (Elmore & Ranney, 1954). Nevertheless, damage from female feeding and oviposition is generally minor in comparison with the more pro‐ nounced mining activity of larvae as they feed within leaves and stems of plants. Larval feeding not only reduces the marketability of plants because of the aesthetic damage, but it also reduces the photosynthetic capacity of plants, which reduces plant vigor, growth and yield (Al-Khateeb & Al-Jabr, 2006; Trumble et al., 1985). Sufficiently high densities of larvae can lead to defoliation. Leafminer caused defoliation can lead to significant losses in fruiting crops because the fruit becomes exposed to sunscald damage from the loss of the plant cano‐ py (Schuster & Everett, 1983). On a per capita basis, *Liriomyza huidobrensis* has the most sig‐ nificant effect on host plants because it creates large mines in the spongy mesophyll of foliage and in petioles (Parrella et al., 1985). It is also known to mine pods of pea plants (*Pisum sativum* L.) (CABI, 2004). In contrast, *L. trifolii* and *L. sativae* tend to mine only

In addition to the direct damage inflicted to crop plants, producers may suffer further eco‐ nomic losses because of quarantine restrictions that constrain international trade (Gitonga et al., 2010). Producers lose export markets when importing countries ban products because of the actual or potential presence of leafminer infestations in the country of origin. Even with‐ out complete bans, phytosanitary measures (e.g., fumigation or irradiation (Hallman et al., 2011)) required by importing countries may make exports cost prohibitive for producers in

One of the great challenges in understanding the pest status of *Liriomyza* spp. and effectively managing them has been the uncertainty regarding taxonomy and misidentification of pest species. Agromyzidae species occur throughout the world, and many species are morpho‐ logically similar, making distinctions among species difficult. Minkenberg (1988a) suggests that as a consequence invasive populations of *L. trifolii* became well established in some countries because specimens of early colonizers were misidentified as native species, and so no management programs were adopted. More thorough species determinations were not

Among the three major pest species, there have been considerable historical problems with their taxonomy and identification. *Liriomyza sativae* was originally described from Argentina by Blanchard (1938) and is thought to be endemic to regions of South and North America (Spencer, 1973). It was recorded as a pest of numerous horticultural crops in southern Florida (USA) by the 1940s. Many early records of *Liriomyza* pests in Florida, USA refer to *Liriomyza pusilla* (Meigen) although the actual species of concern was almost certainly *L. sativae* (Spencer, 1973). *Liriomyza sativae* has probably been

through the upper palisade mesophyll of foliage.

234 Insecticides - Development of Safer and More Effective Technologies

**2. Taxonomy, origins and invasiveness**

undertaken until widespread crop losses were reported by growers.

the country of origin.

The endemic range of *L. trifolii* is thought to encompass eastern North America, the Carib‐ bean Basin, and parts of South America, although this range must be interpreted cautiously, again because of historical taxonomic uncertainty (Scheffer & Lewis, 2006; Spencer, 1965; 1973). Spencer (1965) noted that *L. trifolii* was widespread throughout Florida but did not consider it to be as significant of a pest as *L. sativae* at that time*.* The *L. trifolii* discussed by Frick (1959) as occurring in the western USA (California, Oregon, Washington) was later de‐ termined to be a new species, *L. fricki* Spencer (1965).

*Liriomyza huidobrensis* was first described, as *Agromyza huidobrensis,* from specimens reared from *Cineraria* in Argentina (Blanchard, 1926). For many years, *L. huidobrensis* was considered to be endemic to North America and to South America, although it was not recorded from Central America (Parrella, 1982; Spencer, 1973). In North America, this species was considered to be present in the far western states of the United States (Cali‐ fornia, Hawaii, Oregon, and Washington) (Spencer, 1973), but recent molecular research has confirmed that this North America taxon is a distinct species, *Liriomyza langei* Frick (Scheffer, 2000; Scheffer & Lewis, 2001).

Adding to the taxonomic complexity regarding *Liriomyza* is the recent discovery that *L. sati‐ vae* and *L. trifolii* are each composed of biologically distinct cryptic species (Scheffer & Lewis, 2005; 2006). There is evidence that other pest *Liriomyza* species may also be composed of bio‐ logically distinct cryptic species (Lonsdale, 2011; Morgan et al., 2000; Reitz & Trumble, 2002b). Genetic and ecological differences among such cryptic species have important impli‐ cations for understanding the pest status and management of these species (Rosen, 1978; Scheffer & Lewis, 2005).

In addition to our evolving understanding of the taxonomy of *Liriomyza,* the history of *Liriomyza* spp. as pests has changed substantially over time. Although leafminers have been recognized as pests for many years, they remained relatively minor pests in limited geographic areas through the early 20th century (Hills & Taylor, 1951). In Florida, prob‐ lems with leafminer control began to appear in the 1940s, which coincides with the ad‐ vent of the use of synthetic insecticides (Hayslip, 1961; Wene, 1953). The initial species to cause these problems was *L. sativae* (Spencer, 1973). From the 1940s through the 1970s, there were repeated failures of insecticides to control leafminers in Florida (Hayslip, 1961; Levins et al., 1975; Wolfenbarger, 1954) and in the Rio Grande Valley of Texas (Wene, 1953), leading to substantial crop damage periodically. By the late 1970s, *L. trifolii* had become the predominant leafminer pest in Florida, and it soon became the most im‐ portant pest of tomato (*Solanum lycopersicum* L.) in the state (Waddill et al., 1986). This sudden explosion of leafminer problems led growers to intensify insecticide treatments in attempts to manage the problems. Waddill et al. (1986) note that soon after the out‐ break of *L. trifolii* growers were making three or more insecticide applications per week against leafminers with little success in managing the problem.

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

(Minkenberg, 1988a). Today, *L. trifolii* is widespread throughout Europe, Africa and Asia. In the Americas, invasive populations have probably been introduced into regions where

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

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

237

Whereas *L. trifolii* has invaded many European countries, *L. sativae* has a more restricted dis‐ tribution in Europe. It has been more widespread than *L. trifolii* in Asia and in Oceania, even though its presence was not recorded before the early 1990s. However, this distribution may be changing as *L. trifolii* invades more areas of Asia. For example, in the Chinese province of Hainan, *Liriomyza* spp. have been the predominant pest of cowpea, *Vigna unguiculata* L. Walpers, since 1993 when *L. sativae* first invaded the island and spread to other provinces. Subsequently, *L. trifolii* invaded Hainan in 2006, which has lead to the displacement of *L. sat‐ ivae* (Gao et al., 2011). In contrast to the displacements of *L. sativae* by *L. trifolii*, *L. sativae* appears to have recently displaced *L. trifolii* as the predominant species in Japanese vegeta‐

*Liriomyza huidobrensis* has spread rapidly through the world since the late 1980s when it was first recorded throughout Europe (reviewed in Weintraub & Horowitz, 1995). By the mid 1990s, it was well established throughout Asia, Africa and Central America (He et al., 2002; Scheffer et al., 2001; Shepard et al., 1998). It is not known at this time if *L. hui‐ dobrensis* has displaced either *L. sativae* or *L. trifolii* in any geographic region. Where these species co-occur, changes in demographics have been linked to climatic conditions, with *L. huidobrensis* predominating in cooler seasons or at higher elevations with cooler climates (Mujica & Kroschel, 2011; Tantowijoyo & Hoffmann, 2010; Weintraub, 2001a). Although *L. langei* has become a significant pest in California, it has not become an inva‐

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‐

the species is indigenous (Minkenberg, 1988a).

ble crops (Abe & Tokumaru, 2008).

sive species to date (Scheffer et al., 2001).

**3. Biological influences on pest status**

*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‐ cide resistant populations.

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 plant material (Minkenberg, 1988a).

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

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 (Minkenberg, 1988a). Today, *L. trifolii* is widespread throughout Europe, Africa and Asia. In the Americas, invasive populations have probably been introduced into regions where the species is indigenous (Minkenberg, 1988a).

Whereas *L. trifolii* has invaded many European countries, *L. sativae* has a more restricted dis‐ tribution in Europe. It has been more widespread than *L. trifolii* in Asia and in Oceania, even though its presence was not recorded before the early 1990s. However, this distribution may be changing as *L. trifolii* invades more areas of Asia. For example, in the Chinese province of Hainan, *Liriomyza* spp. have been the predominant pest of cowpea, *Vigna unguiculata* L. Walpers, since 1993 when *L. sativae* first invaded the island and spread to other provinces. Subsequently, *L. trifolii* invaded Hainan in 2006, which has lead to the displacement of *L. sat‐ ivae* (Gao et al., 2011). In contrast to the displacements of *L. sativae* by *L. trifolii*, *L. sativae* appears to have recently displaced *L. trifolii* as the predominant species in Japanese vegeta‐ ble crops (Abe & Tokumaru, 2008).

*Liriomyza huidobrensis* has spread rapidly through the world since the late 1980s when it was first recorded throughout Europe (reviewed in Weintraub & Horowitz, 1995). By the mid 1990s, it was well established throughout Asia, Africa and Central America (He et al., 2002; Scheffer et al., 2001; Shepard et al., 1998). It is not known at this time if *L. hui‐ dobrensis* has displaced either *L. sativae* or *L. trifolii* in any geographic region. Where these species co-occur, changes in demographics have been linked to climatic conditions, with *L. huidobrensis* predominating in cooler seasons or at higher elevations with cooler climates (Mujica & Kroschel, 2011; Tantowijoyo & Hoffmann, 2010; Weintraub, 2001a). Although *L. langei* has become a significant pest in California, it has not become an inva‐ sive species to date (Scheffer et al., 2001).
