Cien. Inv. Agr. 34(3): 125-142. 2007 www.rcia.puc.cl

LITERATURE REVIEW

Leafminer parasitoids and pest management

Adriana Salvo1 and Graciela R. Valladares Centro de Investigaciones Entomológicas de Córdoba, Instituto Multidisciplinario de Biología Vegetal. Consejo Nacional de Investigaciones Científi cas y Tecnológicas. Facultad de Ciencias Exactas, Físicas y Naturales. Universidad Nacional de Córdoba. Av. Vélez Sarsfi eld 1611. X5016GCA. Córdoba, Argentina.

Abstract

A. Salvo, and G.R. Valladares. 2007. Leafminer parasitoids and pest management. Cien. Inv. Agr. 34(3):125-142. Leafminers are whose larvae live and feed within plant leaves, consuming mesophyll tissue without damaging the leaf epidermis. Several species are considered serious pests on intensive, horticultural, and ornamental crops. Natural enemies are the most frequent source of mortality for this herbivore guild, with parasitoids being the most effective and best represented source. This article provides an updated summary of the available research on leafminer parasitoids in relation to pest management. Parasitoids of leafminers are predominantly generalists, and can thus rapidly include in their host ranges newly introduced leafminer species, frequently achieving effective regulation a few years after the pest becomes established. Classical and augmentative biological control strategies are broadly used for leafminer pest management. Several studies have dealt with the simultaneous use of parasitoids together with chemical and cultural control. Many conventional insecticides have detrimental effects on parasitoids; however, others could be compatible with biological control. Although integrated pest management programs employing a combination of several control strategies have achieved success against leafminer pests, the effects of cultural practices that could boost parasitoid populations have been scarcely studied.

Key words: Biological control, chemical control, cultural control, leafminers, parasitoids, pest management.

Introduction to their hosts’ particular conditions of life, and have great potential in biological pest control Parasitoids are insects with a complex and programs (Hawkins et al., 1993). fascinating biology, whose larvae feed on other insects, killing them in order to complete This article includes a review of leafminer parasit- their development. Although they are usually oids in the context of their potential use in insect unnoticed due to their small size, this group pest management. For this, we reviewed the eco- of organisms has tremendous economic logical literature referring to both theoretical and importance, as they regulate the population of practical aspects that must be considered when their hosts and thereby represent useful tools for using leafminer parasitoids as population regula- insect pest management. Leafminer parasitoids tors. Likewise, other strategies used in the control constitute an interesting and relatively well- of leafminers are discussed, with an emphasis on studied group of species belonging to at the relationship between these methods and the least ten families of the Order Hymenoptera, regulation exercised by the parasitoids. The sub- Suborder Apocrita. These insects have adapted ject is introduced with a brief characterization of leafminer insects, their economic importance, the reasons why several species reach pest status in

Received 07 June 2007. Accepted 23 July 2007. various crops, and the relative importance of par- 1Corresponding author: [email protected] asitoids for the regulation of their populations. 126 CIENCIA E INVESTIGACION AGRARIA

The leafminers the same time, leafminer adults have developed resistance, going from being secondary pests to Leafminers are insects whose larvae live and becoming primary pests (Murphy and La Salle, feed inside the leaves, consuming the mesophyll 1999; Civelek and Weintraub, 2003). Concrete without damaging the leaf epidermis. Their examples of this are Liriomyza sativae (Hills feeding tracks (“mines”) are externally visible and Taylor, 1951), L. trifolii (Reitz et al., 1999), in leaves, as whitish or grey areas with variable leafminers of the Phyllonorycterr on fruit shapes that rangefrom narrow linear galleries trees (Maier, 2001), and several leafminer pests to wide chambers (Hering, 1951). The leaf on tomatoes (Gelenter and Trumble, 1999). mining habit has been developed by a group of over 10,000 species of holometabolous Another factor that could contribute to certain insects, concentrated in four orders: Diptera, leafminer species becoming pests is the Coleoptera, Hymenoptera, and increase in monocultivation. Many parasitoids (Connor and Taverner, 1997). have preference for specifi c plants. Therefore, if the only crop present is not attractive The galleries excavated by the leafminer larva for the parasitoids, leafminers may escape can reduce the photosynthetic capacity of leaves, parasitoidism in this environment (Murphy and cause premature leaf abscission, and permit La Salle, 1999). Finally, the increase of extensive pathogen entry into plant tissue. Moreover, they horticulture and plant commercialization reduce the esthetic value of ornamental plants without appropriate quarantine controls has or edible leaves (Spencer, 1973; Parrella and also favored the expansion of leafminer pest Jones, 1987; Minkenberg and Van Lenteren, distribution. 1986; Maier, 2001; Valladares, in press). Many species are considered pests in several parts of Causes of leafminer mortality the world. Among these are the citrus leafminer Phyllocnistis citrella Stainton (Lepidoptera: Intraspecifi c competition, both direct by ), and more than 100 species interference, or indirect or exploitive, represents of leaf mining fl ies (Diptera: Agromyzidae), an important cause of mortality for the leafminer especially Liriomyza trifolii (Burgess) and larvae (Faeth, 1990; Auerbach et al., 1995; Eber, Liriomyza huidobrensis (Blanchard) in 2004). Leaf abscission has also been indicated horticultural crops, and Agromyza frontella as another important survival factor for (Rondan) in alfalfa (Amalin, et al. 2002; leafminers (Potter, 1985; Faeth, 1990; Girardoz Dempewolf, 2004). et al., 2006a). Abscission can be interpreted as the plant defense induced by leafminer attack. Most authors agree that a leafminer species Nevertheless, in some cases, it could benefi t becomes a pest due to insecticide resistance the leafminers by freeing them from potential development and the elimination of their parasitoid attack (Kahn and Cornell, 1989). On natural enemies. The latter is a consequence of the other hand, some leaf mining larvae release aggressive agricultural practices (i.e. plowing, cytokinins that maintain green areas (“green breaking up, and burning of soils, etc.) and the use islands”) in ageing leaves, which allows them of agrochemicals (Spencer, 1973; Minkenberg to complete their development. Stiling and and Van Lenteren, 1986). Furthermore, another Simberloff (1989), after studying the mortality two factors can importantly contribute to of some species that induce leaf abscission, elevate leafminer population sizes: 1. Relative conclude that this phenomenon must be seen, inconspicuousness, allowing them to go from a parsimonious point of view, as a simple unnoticed until reaching high densities (Maier, response of the plant to the phytophagous 2001), and 2. The protection of their immature damage. Other plant defense mechanisms, stages inside plant tissue, especially against mostly related to chemical and physical aspects, the effects of contact insecticides. This last have also been mentioned (Valladares and characteristic has promoted the indiscreet use Lawton, 1991). of wide spectrum insecticides, which have decimated their natural enemy populations. At The action of natural enemies occurs by VOL 34 N˚3 SEPTEMBER - DECEMBER 2007 127 predation and parasitoidism. Predation has been parasitoids (Hochberg and Hawkins, 1992). cited as the greatest cause of mortality at the On the other hand, leafminers are herbivorous beginning of the growing season of some crops, insects characterized by a distinct homogeneity while parasitoidism is more important in more of both ecological and taxonomic aspects advanced stages of crop development (Queiroz, (Connor and Taverner 1997), which facilitates 2002; Urbaneja et al., 2000). Except for some the development of a diverse community of leafminers, such as Tuta absoluta (Lepidoptera: parasitoids that share hosts, and would explain Gelechiidae), very low mortality values due to why this insect group as a whole has an elevated parasitoidism (<1%) and high levels of larval load of parasitic species (Godfray, 1994). mortality due to predation, which can reach up to 80% (Motta Miranda et al., 1998), have been Most of the leafminer parasitoid species reported. correspond taxonomically to the superfamilies Chalcidoidea (Families Eulophidae and Leafminer predators include birds, spiders and Pteromalidae), Ichneumonoidea (Family insects. Among the insects, there are predators Braconidae), and Cynipoidea (Family Figitidae) in various families of Coleoptera (ej. Carabidae, (Salvo, in press). These insects may be classifi ed Cicindelidae, Staphylinidae), Hemiptera (i.e. as idiobionts, when they permanently paralyze Anthocoridae, Nabidae, Lygaeidae), and their host when ovipositing, or as koinobionts, Hymenoptera (i.e. ants) (Cisneros and Mujica, which only temporarily paralyzes the host, 1998; Motta Miranda et al., 1998; Arno et al., allowing it to continue its development prior to 2003; Grabenweger et al., 2005). The effect provoking its death (Askew and Shaw, 1986). of predators sometimes surpasses the effect of The idiobiont/koinobiont dichotomy would parasitoidism (Memmott et al., 1993; Queiroz, be associated with a series of differentiating 2002; Xiao et al., 2007); furthermore, they can characteristics related to their host group’s even have an adverse effect on the mortality preference, feeding specifi city, reproductive caused by parasitoids (Sato and Higashi, strategy, development time, competitive 1987). capacity, presence of sexual dimorphism, etc. (Gauld and Bolton, 1988; Salvo and Valladares, Although the relative infl uence of predators and 1999). parasitoids in regulating different leafminer species is variable, the literature indicates The idiobionts, by permanently paralyzing their that, in general, the parasitoids constitute hosts, risk the possibility that their food resource the most important group (Parrella, 1987; will later be attacked by other organisms, Hespenheide, 1991). Parasitoids have a key so they are more frequently associated with function in leafminer population control in endophytophagous insects, which feed inside natural ecosystems and in cultivated areas plant tissues and are better protected from with a rational use of insecticides (Lewis et al., unfavorable conditions (Quicke, 1997). On the 2002). other hand, by attacking a resource without physiological defenses, the idiobionts could The leafminer parasitoids consume a greater variety of hosts.

The leafminers are in the phytophagous guild Conversely, the koinobionts must coexist (group of organisms that consume the same for some time with an active organism and, resource in the similar manner), which has the therefore, are restricted to fewer host species. greatest number of parasitoid species per host Since leafminers are endophagous insects, it species, and has the highest average rate of is expected that their parasitic complexes will parasitoidism (Hawkins, 1994). Characteristics be dominated by idiobiont species (Hawkins, of leafminer habits, such as the scarce mobility 1994), which is not always the case (Salvo, of the larvae, the clear visibility of the mines 1996). produced, and the scarce physical protection provided by the leaf epidermis, are the In terms of food specifi city, the literature main causes of leafminers’ vulnerability to contributes abundant evidence that leafminer 128 CIENCIA E INVESTIGACION AGRARIA parasitoids have ample food ranges, generally expected mortality levels (Grabenweger, 2004), defi ned by the host ecology (Godfray, 1994; which may be due to poor synchronization Salvo and Valladares, 1999). This wide food between pests and parasitoids, or to the lack range has interesting consequences regarding of density-dependent responses (degree of introduced species management, since it allows response dependent on population density) the leafminer parasitoids present in an area (Malausa, 1997; Girardoz et al., 2006b). to incorporate the invasive species into their spectrum of hosts in relatively short periods of The effi ciency of parasitoids as agents of time (Murphy and La Salle, 1999). In effect, leafminer mortality varies depending on when a leafminer species invades a new region the species, and it may even vary between and becomes a pest, it initially possesses a low different larval stages of the same species, as number of associated parasitic species, and they well as in relation to environmental conditions are mostly generalist idiobionts with low rates of (Grabenweger, 2003). For example, parasitoids parasitoidism. However, the new leafminers are are likely to be a more important cause of soon colonized by other parasitoids and reach mortality in temperate zones than in the tropics total parasitoidism levels similar to that of native (Hawkins et al., 1997; Queiroz, 2002). Similarly, leafminers, which is often suffi cient to achieve parasitoidism rates would be higher at the end natural control. For example, this process has of the growing season, at least in cultivated been observed in Phyllocnistis citrella Stainton systems (Parrella, 1987; Murphy and La Salle, (Lepidoptera: Gracillariidae) in diverse regions 1999; Urbaneja et al., 2000). The presence of of the world (Uygun et al., 1997; Urbaneja et al., other organisms may also affect leafminer 2000; Amalin et al., 2002; Vercher et al., 2005; parasitoidism rates; in this regard, there is Diez et al., 2006). However, on occasion, the evidence of effects caused by other herbivorous recruiting of a parasitic complex similar to that insects, such as externally chewing herbivores of other leafminers is not accompanied by the (Faeth, 1985), and even by the presence of endophytic fungi (Preszler et al., 1996).

Tritrophic plant-herbivore-parasitoid interac- tions are important in these systems (Price et al., 1980). It has been observed that parasitoidism may also vary depending on plant species (Olivera and Bordat 1996; Rauf and Shepard, 1999), or even between cultivars or genotypes of the same plant species in which the leafminer develops (Fritz et al., 1997; Braman et al., 2005). For example, L. huidobrensis parasitoidism in potato is very low compared to that observed in other crops (Shepard et al., 1998). According to Johnson and Hara (1987), effective biological B control of certain leafminers may depend on the plant species on which the leafminer feeds. One aspect related to the leafminer host plant that may affect their parasitoidism level, mentioned earlier, is leaf abscission. In some cases, leaf abscission causes mortality to both the leafminer and parasitoid (Potter, 1985), while in other systems, the abscission reduces larvae parasitoidism due to the fact that parasitoids don’t search for hosts in fallen Figure 1. Leafmine of Liriomyza commelinae (Frost) leaves (Kahn and Cornell, 1989). (Diptera: Agromyzidae). A. Leafmine onCommelina erecta L. (Commelinaceae). B. Female parasitoid, Chrysocharis fl acilla (Hymenoptera: Eulophidae) searching for its host. Finally, other factors that affect leafminer VOL 34 N˚3 SEPTEMBER - DECEMBER 2007 129 parasitoidism include: droughts (Staley et al., can also affect other aspects in the parasitoid- 2006), leaf age (Facknath, 2005), and leafminer leafminer relationship, like searching behavior position in the plant (Barrett, 1994; van der (Connor and Cargain, 1994). Linden 1994; Brown et al., 1997). Biological control In parasitoid insects, as well as parasitoidism itself, there are two other behaviors that may Cases of leafminer biological control, cited in increase leafminer mortality: 1. feeding on the the literature, mainly report on the introduction host (host feeding) and 2. host paralyzation and augmentative release of parasitoid insects, without oviposition or feeding (host stinging). although other organisms have also been employed, such as nematodes and bacteria In the fi rst case, adult wasps feed on a certain (Sher et al., 2000; van Mele and van Lenteren proportion of leafminer larvae, which may or 2002; Cikman and Comelkcloglu, 2006). There may not be a previous requisite for egg laying are numerous successful examples of classic (Jervis and Kidd, 1986). Some parasitoids use biological control (introduction of agents for hosts of different sizes, either as a substrate for the control of a native or foreign pest) with egg laying or to feed upon (Duncan and Peña, parasitoids for different species of leafminers, 2000). The magnitude of the mortality due to both in the open fi eld (Dharmadhikari et al., host feeding may be similar to, or even higher 1977; Johnson et al., 2003; García-Marí et al., than, that caused by the parasitoidism itself 2004) and in greenhouses (van Lenteren and (Amalin et al., 2002; Bernardo et al., 2006). Woets, 1988; Heinz and Parrella, 1990; Abd- However, the effect of host feeding, functionally Rabou, 2006). In these cases, studies prior comparable to predation, is frequently ignored. to introduction are important and include This may greatly underestimate the levels of tolerance to humidity, ability to recognize mortality caused by parasitoid species (Cure previously parasitized hosts, existence of and Cantor, 2003). alternative hosts, as well as synchronization with the host (Wang et al., 1999; Grabenweger, In some leafminer parasitoid species, particu- 2004; Girardoz et al., 2006b; Zappala and larly belonging to the genera Diglyphus Walker, Hoy, 2004). Temperature constraints have also Sympiesis Foerster and Pnigalio Schrank been shown to be an obstacle for a leafminer (Hymenoptera, Eulophidae), paralyzation and parasitoid to be successfully introduced in death of leafminer larvae are often observed some regions (Klapwijk et al., 2005; Llácer et without them being used as an ovipositon al., 2006). substrate or to feed on (Casas, 1989). This behavior, interpreted as a way to decrease Large-scale rearing of parasitoids for leafminer the number of leafminer larvae in the plant control has been considered in the literature to ensure the survival of the parasitized ones, (Parrella et al., 1989; Kharrat and Jerraya, varies with the size of the hosts availability, 2005). Diverse factors have been mentioned their density, the size of cages in which the as important at the time of carrying out large- parasitoids are reared, and temperature (Heinz scale rearing, among which can be highlight and Parrella, 1989; Patel and Schuster, 1991; humidity, photoperiod, and temperature (Yoder Patel et al., 2003). and Hoy 1998; Urbaneja et al., 2001; Lim et al., 2006; Kafl e et al., 2005; Haghani et al., 2007). Density-dependence in parasitoidism is a phenomena usually considered favorable for Large-scale rearing of parasitoids implies host population regulation to be effective simultaneous management of three trophic (Connor and Beck, 1993; Eber et al., 2001). In levels, which can be diffi cult (Smith and Hoy, some cases, the parasitoidism caused by native 1995). The costs and benefi ts for rearing parasitoids is more coupled to the density of an parasitoids should be carefully analyzed, and exotic leafminer than the parasitoidism caused various modifi cations have been proposed by the parasitoids introduced for their control in order to get positive results based on (Amalin et al., 2002). The density of hosts conventional techniques (Rizqi et al., 1999). The 130 CIENCIA E INVESTIGACION AGRARIA overproduction of males in large-scale parasitoid species would be more effective in regulating rearing increases the costs of biological control the pest than various species. Some studies because only females kill the hosts. For this, using leafminer parasitoids indicate that two techniques have been developed to signifi cantly species released together do not control the host increase the proportion of females by means of better than when releasing only one (Bader et using different sized hosts (Ode and Heinz, al., 2006). To establish a priori the feasibility 2002; Chow and Heinz, 2006). of multiple introductions, various laboratory studies have been carried out to determine The size of the leafminers may not only affect the role of competition and interference in the sex ratio but also the size of the parasitoids leafminer parasitoids (Heimpel and Meloche, reared on them, which could have consequences 2001; Urbaneja et al., 2003; Mitsunaga and on their reproductive capacity (Abe et al., 2005). Yano, 2004), and also the possible interaction Intraspecifi c differences in body size have been between predators and parasitoids (Wu and observed, for both parasitoids that develop in Lin, 1998). different host species (Salvo and Valladares, 1996), as well as for those that parasitoidize The simultaneous introduction of parasitoids the same polyphagous leafminer species and nematodes has been analyzed, with that reach different body sizes on different confl icting results: in some cases, parasitized host plants (Salvo and Valladares, 2002). leafminer larvae were infected by the nematode, Studies on Diglyphus websteri (Crawford) which reduced the survival of the leafminer and (Hymenoptera: Eulophidae) laboratory rearing the parasitoid as well (Head et al., 2003), while demonstrated the effects of temperature, host in other cases, there was compatibility between species, and sex ratio on the size and other the parasitoids and nematodes (Shanower et growth parameters of the species reared. al., 1992). A crucial element could be the time Complicated interactions between sex ratio- at which each enemy is released in the fi eld. temperature, host-temperature, and host- sex There are examples in which the application ratio-temperature (Bazzocchi et al., 2003) have of nematodes after the release of parasitoids been also observed. . increased the degree of control, but when applied before the impact was negative (Sher et A decrease in the proportion of males can be al., 2000). In the context of simultaneous use induced through the use of bacteria (Argov et of parasitoids and other organisms, the use of al., 2000). Species of Wolbachia are one of Bacillus thuringiensis is worth mention, and the most ubiquitous bacteria in insects, which has shown good results against some leafminer manipulates the reproduction of the host in species (Khyami-Horani and Ateyyat, 2002), several ways, among which can be mentioned including some positive effects on the parasitoids cytoplasmic incompatibility, male death, (Cikman and Comelkcloglu, 2006). feminization of genetic males, and induction of parthenogenesis (West et al., 1998). It has been Parasitoids and chemical control proposed that infected wasps could be more effi cient as leafminer biological control agents In regard to chemical control, most leafminers (Tagami et al., 2006a,b). are resistant to organophosphorates, carbamates, and pyrethroids, and at the same time, their It is important to keep in mind that adults natural enemies are severely damaged by obtained in the laboratory may exhibit these chemicals, which leave few options for differences in parasitoidism and host-feeding their chemical control. Insecticides that do capacity in relation to adults obtained in the not penetrate the leaf surface are practically fi eld (Arno et al., 2003). Therefore, quality ineffective (Weintraub and Horowitz, 1999). For control studies of parasitoids obtained through this reason, insecticides with good translaminar large-scale rearing methods are required. action (i.e. cyromazine and abamectin) are the most widely used against leafminers (Civelek A long debate, at the time of introducing natural and Weintraub, 2003). Growth inhibitors are enemies, consists in knowing if one single useful in controlling leafminers, and at the same VOL 34 N˚3 SEPTEMBER - DECEMBER 2007 131

Table 1. Studies evaluating the toxicity of several chemical substances for parasitoids of leafminers.

Pesticides Toxicity1 High Moderated Low

Acetamiprid Mafi and Ohbayashi, 2006 Hidrayani et al., 2005 Alanycarb Mafi and Ohbayashi, 2006 Weintraub and Horowitz, 1998 Parrella and Kaspi, 2005 Abamectin Schuster, 1994 Prijono et al., 2004 Villanueva-Jiménez and Hoy, 1998 Weintraub, 1999; Shen et al., 2003 Bjorksten and Robinson, 2005 Parrella and Kaspi, 2005. Bifenthrin Mafi and Ohbayashi, 2006 Carbosulfan Hidrayani et al., 2005 Cloropyrifos Prijono et al.,2004 Clothianidin Mafi and Ohbayashi, 2006 Mafi and Ohbayashi, 2006 Cyromazin Weintraub and Horowitz, 1998 Weintraub, 1999; Shen et al., Weintraub, 1999. 2003; Prijono et al., 2004; Bjorksten and Robinson, 2005 Difl ubenzuron van Driesche et al., 1998 Villanueva-Jiménez and Hoy, 1998; Mafi and Ohbayashi, 2006 Dimetoato Darvas and Andersen, 1999 Dinotefuran Mafi and Ohbayashi, 2006 Etofenprox Saito 2004 Fenoxycarb Parrella et al., 1983; Grenier and Grenier, 1993; Villanueva-Jiménez and Hoy, 1998. Fenvalerato Rathman et al., 1990 Flufenoxuron Shen et al., 2003 Imidacloprid Villanueva-Jiménez and Hoy, 1998; Mafi and Ohbayashi, 2006 Villanueva-Jiménez and Tran et al., 2005 Hoy, 1998. Isoxathion Mafi and Ohbayashi, 2006 Lufenuron Tran et al., 2005 Mancozeb van Driesche et al., 1998 Prijono et al., 2004; Bjorksten and Robinson, 2005 Methomyl Saito, 2004 van Driesche et al., 1998 Rathman et al., 1990 Milbemectin Ohno et al., 1999 Mineral oil Conti et al., 2004, Villanueva-Jiménez and Mafi and Ohbayashi, 2006 Hoy, 1998 Neem and other Conti et al., 2004 Villanueva-Jiménez and natural products Hoy, 1998; Immaraju, 1998; Abou-Fakhr Hammad et al., 2000; Banchio et al., 2003; Chen et al., 2003a; Shen et al., 2003. Organophosphates Villanueva-Jiménez and Hoy, 1998 Rathman et al., 1990 Othion Villanueva-Jiménez and Hoy, 1998 Oxamyl van Driesche et al.,1998 Rathman et al., 1990 Permethrin Saito 2004 Rathman et al., 1990 Pimetrozin Tran et al., 2005 Profenofos Hidrayani et al., 2005 Prothiofos Saito, 2004 Tefl ubenzuron Mafi and Ohbayashi, 2006 Thiamethoxam Mafi and Ohbayashi, 2006

1Given the various approaches used in the studies, three qualitative levels of toxicity were considered: low, parasitoids are not signifi cantly affected; high, parasitoids suffer high mortality and/or population reduction; and moderated, effects are noticeable, but they are not very strong, or are variable among generations, treatments, etc. time, are potentially compatible with biological There are numerous studies on the susceptibility control agents due to their low toxicity and high of leafminer parasitoids to different types specifi city. of insecticides (Table 1). Some species of 132 CIENCIA E INVESTIGACION AGRARIA leafminer parasitoids have developed resistance, biological control in crops. These plant species mainly to organophosphorates. For example, could be used for the implementation of open- Diglyphus begini (Ashmead) (Hymenoptera: fi eld rearing of parasitoids (Parkman et al., Eulophidae) is tolerant to oxamyl, methomyl, 1989), which consist of favoring the presence permethrin, and fenvalerate (Rathman et al., of plants and harmless leafminers, in the same 1990). Insecticide application time and method environment as the crop, to increase populations may affect the susceptibility of the parasitoids of natural enemies. Rearing parasitoids in the (Kaspi and Parrella, 2005; Weintraub, 1999), open fi eld has been successful for controlling which varies between species (Mafi and some leafminers (van der Linden, 1992). For Ohhayashi, 2006) and even between genders this, the knowledge of leafminer host ranges (Rathman et al., 1992). and their parasitoids is critical (Parkman et al., 1989; Chen et al., 2003b; Rizzo, 2003). In some In studies with different leafminer species, cases, the study of trophic webs in different crops treated with low doses or without environments has made possible the theoretical insecticides had higher percentages of proposal of open-fi eld rearing systems, taking parasitoidism (Galantini Vignez and Redolfi de into account the possible interactions between Huiza, 1992; van Driesche et al., 1998; Adachi, the species at three trophic levels (Valladares 2002; Chen et al., 2003a). Likewise, in organic and Salvo, 1999). crops, greater parasitoid species richness along with improved effi ciency has been observed Policultures and planting additional plant (Balázs, 1998). However, in other cases, there species with the main crop may also have a was no difference on leafminer parasitoid positive effect on parasitoids. For example, it densities between plots treated and not has been observed that at the beginning of the treated with synthetic insecticides (Mafi and sweet potato crop cycle, growing kidney bean Ohbayashi, 2004). plants in adjacent strips attracts L. huidobrensis parasitoids, and advances and increases their Parasitoids and cultural control presence in the sweet potato crop (Da Paixão Pereira et al., 2002). Likewise, potato cultivated It is possible to increase the action of leafminer along with wheat has less leafminer damage enemies through habitat management (Price because wheat attracts parasitoids (Ebwongu et and Harbaugh, 1981). Different studies mention al., 2001). the importance of weed patches near crops as possible reservoirs of parasitoids (Murphy and Adult parasitoid food provisioning, by means La Salle, 1999). For this reason, it has been of sugar solutions or honey, is a conservation suggested that the management of weeds and biological control practice that has been other plants in or at the edge of an agroecosystem repeatedly used (Powell, 1986). However, can improve the availability of pollen and nectar in some cases, the provision of food for the for leafminers’ natural enemies (van Mele parasitoids of a primary pest can have a and van Lenteren, 2002). In some cases, the negative impact on the control of secondary presence of fl owering plants in habitats nearby pests, to which leafminers generally belong to produces an increase in leafminer parasitoidism (Mitsunaga et al., 2006). (Chen et al., 2003b). However, in other cases, the increase in plant diversity had no effect on Among biological control techniques that leafminers or their parasitoids (Johnson and augment and conserve leafminers’ natural Mau, 1986; Letourneau, 1995). enemies, physical devices have been designed to allow parasitoids to escape, which are generally Although some weeds may act as reservoirs smaller than their hosts, based on containers of leafminer pests (Smith and Hardman, 1986; with mined leaves (Kehrli et al., 2005). This Schuster et al., 1991), others give refuge to apparatus serve to augment or conserve local or leafminer specialists, which do not harm crops. foreign parasitoid populations and could be a low In the latter case, weeds provide alternative cost alternative to the release of conventionally hosts for the parasitoids, thereby increasing the reared natural enemies. This method can be VOL 34 N˚3 SEPTEMBER - DECEMBER 2007 133 used where chemical control is forbidden, like sticky surfaces, play a double role, monitoring in the case of organic agriculture. By making leafminer populations (to learn the appropriate adjustments in screen size, diverse parasitoid time to apply some type of control), and at the and host systems can be managed in this way same time, decrease the number of leafminers (Kehrli and Bacher, 2004). in a fi eld (Larraín, 2004). These traps are used in integrated pest management programs It is important to keep in mind that although for leafminer fl ies (Agromyzidae), where the some practices recommended that leafminer number and surface area of traps for effective control favor the increase of parasitoid control is known in some detail (Braun and populations, others harm them. For example, Shepard, 1997). However, there is a possibility fl ooding to drown pupae of certain leafminers, that yellow sticky traps decrease parasitoid or sunlight exposition of pupae to provoke their populations (Gonçalves, 2006). The combination death also reduces populations of larvo-pupal of yellow traps with attractive substances for parasitoids (Braun and Shepard, 1997). the leafminers, such as extracts of host plant leaves, notably decreases the capture of other Compost application to the crop may have insects and possibly also reduces the number of an indirect effect on leafminers, increasing parasitoids trapped there (Harand et al., 2004). their predator’s diversity and effi ciency (Brown and Tworkoski, 2004). However, Integrated pest and leafminer management nitrogen fertilizers must be used with care because they can stimulate pest development, The integration of various practices in integrated augmenting not only the plant’s vigor, but also pest management programs has proven to be the survival of leafminer larvae and pupae successful in the control of leafminers. The (van Lenteren and Overholt, 1994). There replacement of synthetic chemical pesticides might be fertilization thresholds above which by biopesticides (i.e. Bacillus thuringiensiss) the numbers of leafminer pupa are augmented or the selective use of insecticides with low and the parasitoidism diminishes, as shown in impact on the natural enemies, the decrease of citrus leafminers (Ateyyat and Mustafa, 2001). disturbances imposed in the system (through On the other hand, elevated levels of nitrogen less aggressive agricultural practices), and fertilization in kidney bean crops decreased the the implementation of the different types of development time and increased the fertility biological control all increase the chances of of the parasitoid Chrysocharis oscidinis controlling leafminers (Murphy and La Salle, (Hymenoptera: Eulophidae) on the leafminer 1999). Liriomyza trifolii (Kaneshiro and Johnson, 1996). Other studies have evaluated the effect Laboratory experiments with cages demonstrate of fertilization on parasitoidism rates, without that the release of Diglyphus isaea together analyzing the mechanisms involved (Yarnes with the release of sterile male L. huidobrensis and Boecklen, 2006). constitutes a more effi cient method than the use of each technique separately (Kaspi and Parrella, One practice recommended for reducing 2006). Some parasitoids can develop in eggs laid leafminer populations is the destruction of by females sterilized by gamma rays, even over plant residues from the previous harvests that several generations (Harwalkar et al., 1987). were attacked by pests, which can be burned or buried (Larraín, 2004), but this practice Diverse studies have undertaken the also reduces parasitoid populations (Vincent et implementation of integrated pest management al., 2004). However, pruning during summer programs for the control of leafminers, and placing the cut branches under the trees including models and detailed costs-benefi t resulted in a decrease in the number of citrus analyses (Dudley et al., 1989; Shepard et al., leafminer larvae and pupae without affecting 1998; Gelernter and Trumble, 1999; Reitz et parasitoidism (Ateyyat and Mustafa, 2001). al., 1999; Motta Miranda et al., 2005). They agree that it is possible to markedly decrease Sticky traps, consisting usually of yellow the amount of pesticides applied compared 134 CIENCIA E INVESTIGACION AGRARIA to calendar applications. For example, the employed for leafminer pest control. integrated pest management programs for L. huidobrensis in Perú include the use of resistant Resumen or tolerant varieties, irrigation management, elimination of harvest waste, sticky yellow Los minadores de hojas son insectos cuyas traps, insecticides with low toxicity, and larvas viven y se alimentan dentro de las hojas, biological control (Palacios et al., 1995). In consumiendo el mesófi lo sin dañar la epidermis greenhouses, the application of adulticides (i.e. foliar. Varias especies son consideradas serias pyrethroids) to reduce the initial populations plagas de cultivos intensivos, hortícolas y of the miner pest, in combination with two ornamentales. Entre las fuentes de mortalidad or three applications of selective insecticides, más importantes para este gremio de fi tófagos such as azadirachtin, minimizes the possibility se citan a los enemigos naturales, de los que se of resistance and ensures the control of all the destacan los parasitoides como el grupo más stages of the pest without obstructing the action efectivo y mejor representado. Este artículo of natural enemies, extending the control range proporciona un resumen actualizado de la (Immaraju, 1998). información disponible sobre parasitoides de minadores de hojas en relación al manejo de Conclusion plagas. Por ser generalistas, los parasitoides de minadores de hojas pueden incluir rápidamente As a conclusion, is important to emphasize that en su rango alimenticio a especies introducidas, there are abundant bibliographic records that muchas veces lográndose un control efectivo detail the relationship between parasitoids and luego de unos pocos años de establecida la leafminers. They include descriptive biological plaga. Control biológico clásico y aumentativo or ecological aspects without direct relation son estrategias ampliamente usadas para regular to the management of pest species, studies las poblaciones de minadores de hojas plaga. which were not included here because they Numerosos estudios abordan la compatibilidad were beyond the objective of this review. Also, del uso de parasitoides con control químico y there are numerous practical studies available cultural. Si bien la mayoría de los insecticidas that analyze the compatibility of parasitoid use convencionales poseen efectos adversos para combined with different chemical pesticides, as los parasitoides, otros serían compatibles con el explained above. control biológico. Se conoce que la combinación de diversas estrategias de control en programas The areas that are less developed are those de manejo integrado de plagas ha resultado that explore the importance of the different efectivo contra minador de hojas plaga. Sin sources of mortality in leafminer life tables embargo, los efectos de prácticas culturales and the impact of agricultural practices on the que podrían favorecer las poblaciones de parasitoid fauna. In this regard, the effect of parasitoides han sido escasamente estudiados. nearby weeds on the parasitoids is practically unknown, and information referring to the Palabras clave: Control biológico, control interaction of pest parasitoids with other cultural, control químico, minadores de hojas, hosts in the agroecosystem is also scarce. parasitoides. To have this type of information available, especially incorporating information on the Acknowledgments three trophic levels involved: plants (cultivation and spontaneous vegetation), leafminers (pest We would like to express our gratitude to the and alternative hosts), and parasitoids, would following institutions that have supported make the implementation of ecologically the development of this research: CONICET, sound management strategies possible. Open- SECYT, FONCYT. We also thank W. A. Quispe fi eld parasitoid rearing systems, management Avalos for reading the original manuscript of plant diversity, and other environmental and M. S. Fenoglio (Entomological Research manipulation methods, constitute, in this sense, Center, Universidad Nacional de Córdoba) for alternatives that have been, up to now, scarcely the photographic work. VOL 34 N˚3 SEPTEMBER - DECEMBER 2007 135

References attacking chrysanthemum Biological Control 39:441-452. Abd-Rabou S. 2006. Biological control of the Balázs, K. 1998. The importance of parasitoids in leafminer, Liriomyza trifolii by introduction, apple orchards Biol. Agric. Hortic. 15:123-129. releasing, evaluation of the parasitoidsDiglyphus Banchio, E., G.R. Valladares, M. Defagó, S. isaea and Dacnusa sibirica on vegetables Palacios, and C. Carpinella. 2003. Effects of crops in greenhouses in Egypt. Archives of Melia azedarach (Meliaceae) fruit extracts on Phytopathology and Plant Protection 39:439- the leafminer Liriomyza huidobrensis (Diptera: 443. Agromyzidae): assessment in laboratory and Abe, Y., T. Takeuchi, S. Tokumaru, and J. Kamata. fi eld experiments. Ann. Appl. Biol. 143:187- 2005. Comparison of the suitability of three pest 193. leafminers (Diptera: Agromyzidae) as hosts Barrett, B.A. 1994. Within-tree distribution of for the parasitoid Dacnusa sibirica (Hym.: blancardellaa(F.) and P. crataegella Braconidae). Eur. J. Entomol. 102:805-807. (Clemens) (Lepidoptera: Gracillariidae) and Abou-Fakhr Hammad, E.M., N.M. Nemer, and associated levels of parasitism in commercial N.S. Kawar. 2000. Effi cacy of the Chinaberry apple orchards. Biol. Control 4:74-79. tree (Meliaceae) aqueous extracts and certain Bazzocchi, G.G., A. Lanzoni, G. Burgio, and M.R. insecticides against the pea leafminer (Diptera: Fiacconi. 2003. Effects of temperature and Agromyzidae). J. Agr. Sci. 134:413-420. host on the pre-imaginal development of the Adachi, I. 2002. Evaluation of generational percent parasitoid Diglyphus isaea (Hymenoptera: parasitism on Lyonetia clerkella (Lepidoptera: Eulophidae). Biol. Control 26:74-82. Lyonetiidae) larvae in peach orchards under Bernardo, U., P.A. Pedata, and G. Viggiani. 2006. different management intensity. Appl. Entomol. Life history of Pnigalio soemius (Walker) Zool. 37:347-355. (Hymenoptera:Eulophidae) and its impact Amalin, D.M., J.E. Peña, R.E. Duncan, H.W. on a leafminer host through parasitization, Browning, and R. Mcsorley. 2002. Natural destructive host-feeding and host-stinging mortality factors acting on citrus leafminer, behavior. Biol. Control 37:98-107. Phyllocnistis citrella, in lime orchards in South Bjorksten, T.A., and M. Robinson. 2005. Juvenile Florida. BioControl 47:327-347. and sublethal effects of selected pesticides Argov, Y., Y. Gottlieb, S. Amin-Spector, and E. on the leafminer parasitoids Hemiptarsenus Zchori Fein. 2000. Possible symbiont-induced varicornis and Diglyphus isaea (Hymenoptera: thelytoky in Galeopsomyia fausta, a parasitoid Eulophidae) from Australia. J. Econ. Entomol. of the citrus leafminer Phyllocnistis citrella. 98:1831-1838. Phytoparasitica 28:212-218. Braman, S.K., G.D. Buntin, and R.D. Oetting. 2005. Arno, J., E. Alonso, and R. Gabarra. 2003. Role of Species and cultivar infl uences on infestation the parasitoid Diglyphus isaea (Walker) and the by and parasitism of a columbine leafminer predator Macrolophus caliginosus Wagner in (Phytomyza aquilegivora Spencer). J. Environ. the control of leafminers. Bulletin OILB/SROP Hortic. 23:9-13. 26:79-84. Braun, A.R., and M. Shepard. 1997. Leafminer Askew, R.R., and M.R. Shaw. 1986. Parasitoid Fly: Liriomyza huidobrensis. Technical Communities: their size, structure and Bulletin. International Potato Center and development. p. 225-264. In: J. Waage and D. Clemson University Palawija IPM Project. Greathead (eds.). Insect Parasitoids. Academic The International Potato Center. .www.eseap. Press, London. cipotato.org/fi le-library.htm (Accessed 2 July, Ateyyat, M.A., and T.M. Mustafa. 2001. Cultural 2007). control of citrus leafminer, Phyllocnistis citrella Brown, M.W., and T. Tworkoski. 2004. Pest Stainton (Lepidoptera:Gracillariidae) on lemon management benefi ts of compost mulch in apple in Jordan. Int. J. Pest Manage. 47:285-288. orchards. Agr. Ecosys. Environ. 103:465-472. Auerbach, M.J., E.F. Connor, and S. Mopper. 1995. Brown, J.L., S. Vargo, E.F. Connor and M.S. Minor miners and major miners: population Nuckols. 1997. Causes of vertical stratifi cation dynamics of leafmining insects. p. 83-110. In: in the density of Cameraria hamadryadella. N. Cappuccino and P.W. Price (eds.). Population Ecol. Entomol. 22:16-25. Dynamics. Academic, San Diego, California. Casas, J. 1989. Foraging behaviour of a leafminer Bader, A.E., K.M. Heinz, R.A. Wharton, and C.E. parasitoid in the fi eld. Ecol. Entomol. 14:257- Bográn. 2006. Assessment of interspecifi c 265. interactions among parasitoids on the outcome Cikman, E., and N. Comelkcloglu. 2006. Effects of inoculative biological control of leafminers of Bacillus thuringiensis on larval serpentine 136 CIENCIA E INVESTIGACION AGRARIA

leafminers Liriomyza trifolii (Burgess) (Diptera:Agromyzidae) pelo parasitóide Opius (Diptera:Agromyzidae) in bean. Pakistan J. sp. (Hymenoptera: Braconidae) na cultura da Biol. Sci. 9:2082-2086. batata com faixas de feijoeiro intercaladas. Cisneros, F., and N. Mujica. 1998. The leafminer fl y Ciência e Agrotécnica, Lavras. 26:955-963. in potato: plant reaction and natural enemies as Darvas, B.A., and A.B. Andersen. 1999 Effects of natural mortality factors. CIP Program Report. cyromazine and dimethoate on Chromatomyia Lima Perú. http:/www.cipotato.org/Market/ fuscula (Zett.) (Dipt.,:Agromyzidae) and its PgmRprts/pr97-98/16leafmi.pdf (Accessed 30 hymenopterous parasitoids. Acta Phytopathol. June, 2007). Hun. 34:231-239. Civelek, H.S., and P.G. Weintraub. 2003. Effects Dempewolf, M. 2004. of Economic of bensultap on larval serpentine leafminers, Importance: Agromyzidae of the World. Liriomyza trifolii (Burgess) (Diptera: Multimedia interactive software. ETI, Agromyzidae), in tomatoes. Crop Prot. 22:479- Amsterdam, The Netherlands. 483. Dharmadhikari, P.R., P.A.C.R. Perera, and T.M.F. Connor, E.F., and M.J. Cargain. 1994. Density- Hassen. 1977. A short account of the biological related foraging behaviour in Closterocerus control of Promecotheca cumingi [Col.: tricinctus, a parasitoid of the leaf-mining , Hispidae] the coconut leaf-miner, in Sri Lanka. Cameraria hamadryadella. Ecol. Entomol. BioControl 22: 3-18 19:327-334. Diez, P.A., J.E. Peña, and P. Fidalgo. 2006. Population Connor, E.F., and M.P. Taverner. 1997. The evolution dynamics of Phyllocnistis citrella (Lepidoptera: and adaptive signifi cance of the leaf-mining Gracillariidae) and its parasitoids in Tafí Viejo, habit. Oikos 79:6-25. Tucumán, Argentina. Fla. Entomol. 89:328- Connor, E.F., and M.W. Beck. 1993. Density related 335. mortality in Cameraria hamadryadella Dudley, N.J.A., R.A.E. Mueller, and J.A. Wightman. (Lepidoptera:Gracillariidae) at epidemic and 1989. Application of dynamic programming for endemic densities. Oikos 66:515-525. guiding IPM on groundnut leafminer in India. Conti, F., R. Fisicaro, A. Lo Genco, S. Colazza, Crop Prot. 8:349-357. and G. Liotta. 2004. An IPM program for Duncan, R., and J.E. Peña. 2000. Fecundity, host Phyllocnistis citrella Stainton in Sicily Citrus stage preferences and the effects of temperature Nurseries. p. 8. Proceedings I International on Pnigalio minio (Hymenoptera:Eulophidae), a Cameraria Symposium Cameraria ohridella parasitoid of Phyllocnistis citrella (Lepidoptera: and other invasive leaf-miners in Europe. Gracillariidae). P. Fl. St. Hortic. Soc. 113:20- Prague, Checoslovaquia. 24. Cure, J.R., and F. Cantor. 2003. Atividade predadora Eber, S., H.P. Smith, R.K. Didham, and H.V. Cornell. e parasítica de Diglyphus begini (Ashm.) 2001. Holly leaf-miners on two continents: what (Hymenoptera:Eulophidae) sobre Liriomyza makes an outbreak species? Ecol. Entomol. huidobrensis (Blanch.) (Diptera: Agromyzidae) 26:124-132. em cultivos de Gypsophila paniculata L. Eber, S. 2004. Bottom-up density regulation in the Neotrop. Entomol. 32:85-89. holly leaf-miner Phytomyza ilicis. J. Anim. Chen, A.D., Z.Q. Chen, K.J. Luo, and S. Miao. Ecol. 73:948-958. 2003a. Effects of some insecticides on fi eld Ebwongu, M., E. Adipala, S. Kyamanywa, C.K. population fl uctuation and parasitism of the Ssekabembe, and A.S. Bhagsari. 2001. Infl uence leafminer parasitoid. J. Yunnan Agric. Univ. of spatial arrangements in maize/Solanum 18:249-252. potato intercrops on incidence of potato aphids Chen, X., F. Lang, Z. Xu, J. He, and Y. Ma. 2003b. The and leaf hoppers in Uganda. Afr. Crop Sci. J. occurrence of leafminers and their parasitoids 9:175-184. on vegetables and weeds in Hangzhou area, Facknath, S. 2005. Leaf age and life history variables Southeast China BioControl 48:515-527. of a leafminer: the case of Liriomyza trifolii on Chow, A., and K.M. Heinz. 2006. Control of potato leaves Entomol. Exp. Appl. 115:79-87. Liriomyza langei on chrysanthemum by Faeth, S.H. 1985. Host leaf selection by leaf miners: Diglyphus isaea produced with a standard or interactions among three trophic levels. Ecology modifi ed parasitoid rearing technique. J. Appl. 66:870-875. Entomol. 130:113-121. Faeth, S.H. 1990. Aggregation of a leafminer, Da Paixão Pereira, D.I., J.C. De souza, L.V. Costa Cameraria sp. nov. (Davis): consequences and Santa-Cecília, P. Rebelles Reis, and M. De Abreu causes. J. Anim. Ecol. 59:569-586. Souza. 2002. Parasitismo de larvas da mosca- Fritz, R.S., S.E. McDonough, and A.G. Rhoads. 1997. minadora Liriomyza huidobrensis Blanchard Effects of plant hybridization on herbivore- VOL 34 N˚3 SEPTEMBER - DECEMBER 2007 137

parasitoid interactions. Oecologia 110: 360-367 Haghani, M., Y. Fathipour, A.A. Talebi, and V. Galantini Vignez, L., and I. Redolfi de Huiza. Baniameri. 2007. Temperature-dependent 1992. Niveles de infestación y parasitismo de development of Diglyphus isaeaa (Hymenoptera: Liriomyza huidobrensis en papa cultivada sin Eulophidae) on Liriomyza sativae (Diptera: aplicación de insecticida. Rev. Per. Entomol. Agromyzidae) on cucumber. J. Pest Sci. 80:71-77. 35:101-106. Harand, W., M. Stolz, and F. Hadacek. 2004. Female García-Marí, F., R. Vercher, J. Costa-Comelles, C. mass trapping: a contribution to Cameraria Marzal, and M. Villalba. 2004. Establishment ohridella control. p. 11. In: International of Citrostichus phyllocnistoides (Hymenoptera: Cameraria Symposium Cameraria ohridella Eulophidae) as a biological control agent for and other invasive leaf-miners in Europe. the citrus leafminer Phyllocnistis citrella Prague. Checoslovaquia. (Lepidoptera: Gracillariidae) in Spain. Biol. Harwalkar, M.R., H.D. Rananavare, and G.W. Control 29:215-226. Rahaikar. 1987. Development of Trichogramma Gauld, I., and B. Bolton. 1988. The Hymenoptera. brasiliensis (Hym.:Trichogrammatidae) on British Natural History Museum. Oxford eggs of radiation sterilized females of potato University Press. Oxford. 332 pp. tuberworm, Phthorimaea operculella (Lep.: Gelernter, W.D., and J.T. Trumble. 1999. Factors in Gelechiidae). BioControl 32:159-162. the success and failure of microbial insecticides Hawkins, B.A. 1994. Pattern and process in host- in vegetable crops. Int. Pest Manag. Rev. 4:301- parasitoid interactions. Cambridge University 306. Press, Cambridge, UK. 190 pp. Girardoz, S., M. Kenis, and D.L.J. Quicke. 2006a. Hawkins, B.A., H.V. Cornell, and M.E. Hochberg. Mortality factors affecting the different 1997. Predators, parasitoids, and pathogens developmental stages of Cameraria ohridella as mortality agents in phytophagous insect Deschka and Dimić in Switzerland. p. 11. In: populations. Ecology 78:2145-2152. International Cameraria SymposiumCameraria Hawkins, B.A., M. Thomas, and M.E. Hochberg. ohridella and other invasive leaf-miners in 1993. Refuge theory and classical biological Europe Prague, Checoslovaquia. control. Science 262:1429-1432. Girardoz, S., M. Kenis, and D.L.J. Quicke. 2006b. Head, J., L.F. Palmer, and K.F.A. Walters. 2003. Recruitment of native parasitoids by an The compatibility of control agents used for exotic , Cameraria ohridella: host- the control of the South American leafminer, parasitoid synchronisation and infl uence of the Liriomyza huidobrensis. Biocontrol Sci. environment. Agr. For. Entomol. 8:48-56. Techn.13:77-86. Godfray, H.C.J. 1994. Parasitoids: Behavioural and Heimpel, G.E., and F. Meloche. 2001 Biological Evolutionary Ecology. Princeton University control of alfalfa blotch leafminer (Diptera: Press. Chichester. USA. 473 pp. Agromyzidae) in Ontario: Status and ecology Gonçalves, M.A.A.C. 2006. Utilizacao de of parasitoids (Hymenoptera: Braconidae, armadilhas cromotropicas na monitorizacao de Eulophidae) 20 years after introduction. Great Liriomyza spp. (Diptera: Agromyzidae) e dos Lakes Entomol. 34:17-26. seus parasitoides, no feijao verde. Boletín de Heinz, K.M., and M.P. Parrella. 1989. Attack Sanidad Vegetal, Plagas. 32:169-174. behavior and host size selection by Diglyphus Grabenweger, G. 2003. Parasitism of different larval begini on Liriomyza trifolii in chrysanthemum. stages of Cameraria ohridella. BioControl Entomol. Exp. Appl. 53:147-156. 48:671-684. Heinz, K.M., and M.P. Parrella. 1990. Biological Grabenweger, G. 2004 Why are native european control of insect pests on greenhouse marigolds. parasitoids not able to control the Horse Environ. Entomol. 19:825-835. chestnut leafminer? 1st International Cameraria Hering, E.M. 1951. Biology of the Leaf Miners. Dr. Symposium Cameraria ohridella and other W. Junk, The Hague. The Netherlands 420 pp. invasive leaf-miners in Europe Prague, Hespenheide, H.A. 1991. Bionomics of leaf-mining Checoslovaquia. pp. 12. insects. Annu. Rev. Entomol. 36:535-560. Grabenweger, G., P. Kehrli, B. SchlickSteiner, F. Hidrayani, Purnomo, A. Rauf, P. Ridland, and A. Steiner, M. Stolz, and S. Bacher. 2005. Predator Hoffmann. 2005. Pesticide applications on complex of the horse chestnut leafminer Java potato fi elds are ineffective in controlling Cameraria ohridella: identifi cation and impact leafminers, and have antagonistic effects on assessment. J. Appl. Entomol. 129:353-362. natural enemies of leafminers. Int. J. Pest Grenier, S., and A.M. Grenier. 1993. Fenoxycarb, a Manag. 51:181-187. fairly new Insect growth regulator: a review of its Hills, O.A., and E.A. Taylor. 1951. Parasitization of effects on insects. Ann. Appl. Biol. 122:369-403. dipterous leaf-miners in cantaloups and lettuce 138 CIENCIA E INVESTIGACION AGRARIA

in the Salt River Valley, Arizona. J. Econ. Gracillariidae) Entomol. Gen. 28:115-120. Entomol. 44:759-767. Khyami-Horani H., and M. Ateyyat. 2002. Effi cacy Hochberg, M.E., and B.A. Hawkins. 1992. Refuges of Jordanian isolates of Bacillus thuringiensis as a predictor of parasitoid diversity. Science against the citrus leafminer, Phyllocnistis 255:973-976. citrella Stainton (Lepidoptera:Gracillariidae). Immaraju, J.A. 1998. The commercial use of Int. J. Pest Manage. 48:297-300. azadirachtin and its integration into viable pest Klapwijk, J, E.S.Martinez, H. Hoogerbrugge, M. control programmes. Pestic. Sci. 54:285-289. Boogert, and K. den Bolckmans. 2005. The Jervis, M.A., and N.A.C. Kidd. 1986. Host-feeding potential of the parasitoid Chrysonotomyia strategies in hymenopteran parasitoids. Biol. formosa for controlling the tomato leafminer Rev. 61:395-434. Liriomyza bryoniae in Dutch tomato Johnson, M.W., and H. Hara. 1987. Infl uence of host greenhouses in winter. Bulletin OILB/SROP. crop on parasitoids (Hymenoptera) of Liriomyza 28:155-158 spp. (Diptera:Agromyzidae). Environ. Entomol. Larraín, P. 2004. Situación de la mosca minadora 16:339-344. Liriomyza huidobrensis (Blanchard) en Johnson, M.W., and R. F. L. Mau. 1986. Effects of cultivos de la papa del cono sur de América intercropping beans and onions on populations y sus perspectivas de manejo integrado. p. of Liriomyza spp. and associated parasitic 5-15. En XXI Congreso de la Asociación Hymenoptera. P. Hawaii Entomol. Soc. 27:95- Latinoamericana de la Papa (ALAP). Valdivia, 103. Chile. Johnson, S.J.D., C. Henne, and W.J. Bourgeois. Letourneau, D.K. 1995. Associational susceptibility: 2003. Biological control of the citrus leafminer effects of cropping pattern and fertilizer on with Ageniaspis citricola (Hymenoptera: Malawian bean fl y levels. Ecol. Appl. 5:823- Encyrtidae) in Louisiana. Proc. Fla. State Hort. 829. Soc. 116:224-226. Lewis, O.T., J. Memmott, J. La Salle, C.H.C. Lyal, Kafl e, L., P.Y. Lai, and Y.F. Chang. 2005. Functional C. Whitefoord, and H.J.C. Godfray. 2002. response of a parasitoid Ganaspidium utilis Structure of a diverse tropical forest insect- (Hymenoptera:Eucoilidae) on the leafminer parasitoid community. J. Anim. Ecol. 71:855- Liriomyza trifolii (Diptera:Agromyzidae). 873. Insect Sci. 12:381-385. Lim, U.T., L.M. Zappalà, and A. Hoy. 2006. Pre- Kahn, D.M., and H.V. Cornell. 1989. Leafminers, release evaluation of Semielacher petiolatus early leaf abscission and parasitoids: a tritrophic (Hymenoptera:Eulophidae) in quarantine interaction. Ecology 70:1219-1226. for the control of citrus leafminer: Host Kaneshiro, L.N., and M.W. Johnson. 1996. Tritrophic discrimination, relative humidity tolerance, and Effects of Leaf Nitrogen on Liriomyza alternative hosts Biol. Control 36:65-73. trifolii (Burgess) and an associated parasitoid Llácer, E., A. Urbaneja, A. Garrido, and J. Jacas. Chrysocharis oscinidis (Ashmead) on Bean. 2006. Temperature requirements may explain Biol. Control 6:186–192. why the introduced parasitoid Quadrastichus Kaspi, R., and M.P. Parrella. 2005. Abamectin citrella failed to control Phyllocnistis citrella compatibility with the leafminer parasitoid in Spain. BioControl 51:439-452. Diglyphus isaea. Biol. Control 35:172–179. Mafi , S.A., and N. Ohbayashi. 2004. Seasonal Kaspi, R., and M.P. Parrella. 2006. Improving the prevalence of the citrus leafminer, Phyllocnistis biological control of leafminers (Diptera: citrella Stainton (Lepidoptera:Gracillariidae) Agromyzidae) using the sterile insect technique. and its parasitoids in controlled and uncontrolled J. Econ. Entomol. 99:1168-1175. Citrus iyo groves in Ehime Prefecture, Japan. Kehrli, P., and S. Bacher. 2004. Mass-hatching Appl. Entomol. Zool. 39:597-601. devices: a new biocontrol technique to augment Mafi , S.A., and N. Ohbayashi. 2006. Toxicity parasitoids. p. 118-121 IV California Conference of insecticides to the citrus leafminer, on Biological Control. Berkeley, California, Phyllocnistis citrella, and its parasitoids, USA. Chrysocharis pentheus and Sympiesis striatipes Kehrli, K., M. Lehmann, and S. Bacher. 2005. Mass- (Hymenoptera:Eulophidae) Appl. Entomol. emergence devices: a biocontrol technique for Zool. 41:33-39. conservation and augmentation of parasitoids. Maier, C.T. 2001. Exotic lepidopteran leafminers Biol. Control 32:191-199 in North American apple orchards: rise to Kharrat, S., and A. Jerraya. 2005. Rearing parasitoids prominence, management, and future threats. by mass production of citrus leafminer Biol. Invasions 3:283–293. larvae, Phyllocnistis citrella (Lepidoptera: Malausa, J.C. 1997. Etat d’avancement de la lutte VOL 34 N˚3 SEPTEMBER - DECEMBER 2007 139

biologique classique contre la mineuse des un programa MIP con énfasis en el control agrumes, Phyllocnistis citrella (Stainton) en de mosca minadora en el Valle de Tambo, France. Bulletin OILB/SROP 20:78-80. Arequipa, Perú. p. 21. En: Memorias XVII Memmott, J., H.C.J. Godfray, and B. Bolton. 1993. Reunión ALAP, Mérida, Venezuela. Predation and parasitism in a tropical herbivore Parkman, P., J.A. Dusky, and V.H. Waddill. 1989. community. Ecol. Entomol. 18:348-352. Leafminer and leafminer parasitoid incidence Minkenberg, O., and J. van Lenteren. 1986. The on selected weeds in South Florida. Fla. leafminers Liriomyza bryoniae and L. trifolii Entomol. 72: 569-661. (Diptera:Agromyzidae), their parasites and Parrella, M.P. 1987. Biology of Liriomyza. Annu. host plants: a review. Agricultural University Rev. Entomol. 32:201-224. Wagenigen Papers 86:1-50. Parrella, M.P., and V.P. Jones. 1987. Development Mitsunaga, T., and E. Yano. 2004. The effect of of integrated pest management strategies in multiple parasitism by an endoparasitoid fl oricultural crops. Bull. Entomol. Soc. Am. on several life history traits of leafminer 33:28-34. ectoparasitoids Appl. Entomol. Zool. 39:315- Parrella, M.P., and R. Kaspi. 2005. Effect of 320. abamectin on the leafminer parasitoid Diglyphus Mitsunaga, T. S. Mukawa, T. Shimoda, and Y. isaea. Bulletin OILB/SROP 28:197-200. Suzuki. 2006. The infl uence of food supply Parrella, M.P., G.D. Christie, and K.L. Robb. 1983. on the parasitoid against Plutella xylostella Compatibility of Insect Growth Regulators L. (Lepidoptera:Yponomeutidae) on the and Chrysocharis parksi (Hymenoptera: longevity and fecundity of the pea leafminer, Eulophidae) for the control of Liriomyza trifolii Chromatomyia horticola (Goureau) (Diptera: (Diptera:Agromyzidae). J. Econ. Entomol. Agromyzidae). Appl. Entomol. Zool. 41:277- 76:949-951. 285. Parrella, M.P., J.T. Yost, K.M. Heinz, and G.W. Motta Miranda, M.M.M., M. Picanço, J.C. Zanuncio, Ferrentino. 1989. Mass rearing of Diglyphus and R.N.C. Guedes. 1998. Ecological life table begini (Hymenoptera:Eulophidae) for of Tuta absoluta (Meyrick) (Lepidoptera: biological control of Liriomyza trifolii (Diptera: Gelechiidae). Biocontrol Sci. Techn. 8:597- Agromyzidae). J. Econ. Entomol. 82:420-425. 606. Patel, K.J., D.J. Schuster, and G.H. Smerage. 2003. Motta Miranda, M.M.M., M. Picanço, J.C. Zanuncio, Density dependent parasitism and host-killing L. Bacci, and É.M. da Silva. 2005. Impact of of Liriomyza trifolii (Diptera:Agromyzidae) integrated pest management on the population by Diglyphus intermedius (Hymenoptera: of leafminers, fruit borers, and natural enemies Eulophidae). Fla. Entomol. 86:8-14. in tomato. Ciência Rural 35:204-208. Patel, K.J., and D.J. Schuster. 1991. Temperature Murphy, S.T., and J. LaSalle. 1999. Balancing dependent fecundity, longevity, and host- biological control strategies in the IPM of killing activity of Diglyphus intermedius New World invasive Liriomyza leafminers in (Hymenoptera:Eulophidae) on third instars fi eld vegetables crops. Biocontrol News and of Liriomyza trifolii (Burgess) (Diptera: Information 20:91-104. Agromyzidae). Environ. Entomol. 20:1195- Ode, P.J., and K.M. Heinz. 2002. Host-size- 1199. dependent sex ratio theory and improving Potter, D.A. 1985. Population regulation of the mass-reared parasitoid sex ratios Biol. Control native holly leafminer, Phytomyza ilicicola 24:31-41. Loew (Diptera:Agromyzidae), on American Ohno, K; K. Takesaki, D. Yamaguchi, and H. holly. Oecologia 66:499-505. Takemoto. 1999. Effects of milbemectin Powell, W. 1986. Enhancing parasitoid activity in acaricide on mortality rate of agromyzid crops. In Insect Parasitoids (J. K. Waage and leafminer, Liriomyza trifolii (Burgess), and D. Greathead (eds.). Academic Press, London, its larval parasitoid, Diglyphus isaea (Walker) UK, pp. 319–340. (Hymenoptera:Eulophidae). Japan J. Appl. Preszler, R.W., E.S. Gaylord, and W.J. Boecklen. Entomol. Z. 43:93-97. 1996. Reduced parasitism of a leaf-mining moth Olivera, C.R., and D. Bordat. 1996. Infl uence of on trees with high infection frequencies of an Liriomyza species (Diptera:Agromyzidae) endophytic fungus Oecologia 108:159-166. and their host plants, on oviposition by Opius Price, J.F., and B.K. Harbaugh. 1981. Effect of dissitus females (Hymenoptera:Braconidae). cultural practices on Liriomyza, p. 156-185. Ann. Appl. Biol. 128:399-404. In: D.J. Schuster (ed.). Proc. I FAS Conf. Biol. Palacios, M., J. Tenorio, O. Ortiz, A. Pulcha y R. Control of Liriomyza leafminers. Buena Vista Gomez. 1995. Implementación y difusión de Lake, Florida, U.S.A. 140 CIENCIA E INVESTIGACION AGRARIA

Price, P., C.E. Bouton, P. Gross, B.A. Mac Pheron, Saito, T. 2004. Insecticide susceptibility of the J.N. Thompson, and A.E. Weiss. 1980. leafminer, Chromatomyia horticola (Goureau) Interactions among three trophic levels: the (Diptera:Agromyzidae) Appl. Entomol. Zool. infl uence of plants on interactions between 39:203-208. insect herbivores and natural enemies. Annu. Salvo, A. 1996. Diversidad y e s t r u c t u r a e n c o m u n i d a d e s Rev. Ecol. Syst. 11:41-65. de parasitoides (Hymenoptera:Parasitica) de Prijono, D., M. Robinson, A. Rauf, T. Bjorksten, and minadores de hojas (Diptera:Agromyzidae). A.A. Hoffmann. 2004. Toxicity of chemicals Tesis Doctoral. Facultad de Ciencias Exactas commonly used in Indonesian vegetable crops Físicas y Naturales. Universidad Nacional de to Liriomyza huidobrensis populations and Córdoba, Argentina. 355 p. the Indonesian parasitoids Hemiptarsenus Salvo, A. 2007. Parasitoides de minadores de hojas. varicornis, Opius sp., and Gronotoma En: Biodiversidad de Artrópodos Argentinos micromorpha, as well as the Australian Vol II. Debandi G., Roig S. y L. Claps (eds.). parasitoids Hemiptarsenus varicornis and Sociedad Entomológica Argentina Ediciones. Diglyphus isaea. J. Econ. Entomol. 97:1191- In press. 1197. Salvo, A., and G.R. Valladares 1996. Intraspecifi c Queiroz, J.M. 2002. Distribution, survivorship size variation in polyphagous parasitoids and mortality sources in immature stages (Hymenoptera:Parasitica), of leaf miners and its of the neotropical leaf miner Pachyschelus relation to host size. Entomophaga 40:273-280. coeruleipennis Kerremans (Coleoptera: Salvo, A., and G.R. Valladares. 1999. Parasitoid Buprestidae). Braz. J. Biol. 62:69-76. assemblage size and host ranges in a parasitoid Quicke, D.L.J. 1997. Parasitic Wasps. Chapman and (Hymenoptera)-agromyzid (Diptera) system Hall, London. UK. 470 pp. from Central Argentina. B. Entomol. Res. Rathman, R.J., M.W. Johnson, J.A. Rosenheim, 89:193-197. and B.E. Tabashnik. 1990. Carbamate and Salvo, A., and G.R. Valladares. 2002. Plant-related pyrethroid resistance in the leafminer parasitoid intraspecifi c size variation in three parasitoids Diglyphus begini (Hymenoptera:Eulophidae). J. (Hymenoptera:Parasitica) of a polyphagous Econ. Entomol. 83:2153-2158. leafminer, Liriomyza huidobrensis (Diptera: Rathman, R.J., M.W. Johnson, J.A. Rosenheim, Agromyzidae). Environ. Entomol. 30:874-879. B.E. Tabashnik, and M. Purcell. 1992. Sexual Sato, H. and S. Higashi. 1987. Bionomics of differences in insecticide susceptibility Phyllonorycter (Lepidoptera:Gracillariidae) on and synergism with piperonyl butoxide in Quercus. II. Effects of ants. BioControl 32:53- the leafminer parasitoid Diglyphus begini 60. (Hymenoptera:Eulophidae). J. Econ. Entomol. Schuster, D.J. 1994. Life-stage specifi c toxicity of 85:15-20. insecticides to parasitoids of Liriomyza trifolii Rauf, A., and B.M. Shephard. 1999. Leafminers (Burgess) (Diptera:Agromyzidae). Int. J. Pest in vegetables in Indonesia: surveys of host Manage. 40:191-194. crops, species composition, parasitoids and Schuster, D.J., J.P. Gilreath, R.A. Wharton, and control practices. p. 25-35. In: Lim, G.S., S.S. P.R. Seymour. 1991. Agromyzidae (Diptera) Soetikno and W.H. Loke (eds.) Proceedings of leafminers and their parasitoids in weeds a Workshop on Leafminers of Vegetables in associated with tomato in Florida. Environ. Southeast Asia, Tanah Rata, Malaysia. Entomol. 20:720-723. Reitz, S.R., G.S. Kund, W.G. Carson, P.A. Phillips, Shanower, T.G., J.A. Wightman, A.P. Gutierrez, and J.T. Trumble. 1999. Economics of reducing and G.V. Ranga Rao. 1992. Larval parasitoids insecticide use on celery through low-input pest and pathogens of the groundnut leaf miner, management strategies Agr. Ecosyst. Environ. Aproaerema modicella (Lep.: Gelechiidae), in 73:185-197. India. BioControl 37:419-427 Rizqi, A., E.B. Nadori, M. Abassi, and M. Nia. 1999. Shen, A.D., Z.Q. Chen, K.J. Luo, S. Miao, and Y.H. Comparison of three different rearing methods Yan. 2003. Toxicity of several insecticides to the of Ageniaspis citricola, parasitoid of citrus larvae, eggs, pupae of the leafminer parasitoid, leafminer. p. 247-250. Proceedings 5th World Diglyphus isaea (Hymenoptera:Eulophidae). Congress of the International Society of Citrus Southwest China J. Agric. Sci. 16:69-72. Nurserymen, Montpellier, France. Shepard, B.M., Samsudin, and A.R. Braun. 1998. Rizzo, M.C. 2003. Tritrophic interactions involving Seasonal incidence of Liriomyza huidobrensis Eulophid parasitoids (Hymenoptera, Eulophidae) (Diptera:Agromyzidae) and its parasitoids on of the citrus leafminer Phyllocnistis citrella vegetables in Indonesia. Int. J. Pest Manage. Stainton. Bulletin OILB/SROP 26:39-51. 44:43-47. VOL 34 N˚3 SEPTEMBER - DECEMBER 2007 141

Sher, R.B., M.P. Parrella, and H.K. Kaya. 2000. Urbaneja, A., E. Llácer, A. Garrido, and J. Jacas. Biological Control of the Leafminer Liriomyza 2003. Interspecifi c competition between trifolii (Burgess): Implications for Intraguild two ectoparasitoids of Phyllocnistis citrella predation between Diglyphus begini Ashmead (Lepidoptera:Gracillariidae): Cirrospilus brevis and Steinernema carpocapsae (Weiser). Biol. and the exotic Quadrastichussp. (Hymenoptera: Control 17:155-163. Eulophidae). Biol. Control 28:243-250. Smith, R.M., and J.M. Hardman. 1986. Rates of Uygun, N., N.Z. Elekcioglu, L. Erkilic, I. Karaca, feeding, oviposition, development and survival and U. Kersting. 1997. Studies on biological of Liriomyza trifolii (Burgess) (Diptera: control of Phyllocnistis citrella Stainton (Lep., Agromyzidae) on several weeds. Can. Ent. Gracillariidae) in Turkey. Bulletin OILB/SROP 118:753-759. 20:96-101. Smith, J.M., and M.A. Hoy. 1995. Rearing methods Valladares, G.R. Agromyzidae. 2007. En: for Ageniaspis citricola (Hymenoptera: Biodiversidad de Artrópodos Argentinos Vol II. Encyrtidae) and Cirrospilus quadristriatus Debandi G., Roig S. y L. Claps (eds.) Sociedad (Hymenoptera: Eulophidae) released in a Entomológica Argentina Ediciones. In press. classical biological control program for the citrus Valladares, G.R., and Lawton, J.H. 1991. Host-plant leafminer Phyllocnistis citrella (Lepidoptera: selection in the holly leaf-miner: does mother Gracillariidae). Fla. Entomol. 78:600-608. know best? J. Anim. Ecol. 60:227-240. Spencer, K.A. 1973. Agromyzidae (Diptera) of Valladares G.R., and A. Salvo. 1999. Insect-plant economic importance. Series Ent. 9. Dr W food webs could provide new clues for Pest Junk. The Hague. The Netherlands. 418 pp. Management. Environ. Entomol. 28:539-544. Staley, J.T., S.R. Mortimer, G.J. Masters, M.D. van der Linden, A. 1992. Phytomyza caulinaris Morecroft, V.K. Brown, and M.E. Taylor. 2006. Hering, an alternative host for the development Drought stress differentially affects leaf-mining of an open rearing system for parasitoids of species Ecol. Entomol. 31:460-469. Liriomyza species. P. Sec. Exp. Appl. Entomol. Stiling, P., and D. Simberloff. 1989. Leaf abscission: Neth. Ent. Soc. 3:31-39. induced defence against pests or response to van der Linden, A. 1994. Can biological control damage? Oikos 55:43-49. of Liriomyza spp in glasshouse crops be Tagami, Y., M. Doi, K. Sugiyama, A. Tatara, and improved?. Med. Fac. Landbouww. Univ. Gent. T. Saito. 2006a. Survey of leafminers and 59:297-303. their parasitoids to fi nd endosymbionts for van Driesche, R.G., J.L. Mason, S.E. Wright, improvement of biological control. Biol. Control and R.J. Prokopy. 1998. Effect of reduced 38:210-216. insecticide and fungicide use on parasitism of Tagami, Y., M. Doi, K. Sugiyama, A. Tatara, and T. leafminers (Phyllonorycter spp) (Lepidoptera: Saito. 2006b. Wolbachia-induced cytoplasmic Gracillariidae) in commercial apple orchards. incompatibility in Liriomyza trifolii and its Environ. Entomol. 27:578-582. possible use as a tool in insect pest control. van Lenteren J.C., and W.A. Overholt. 1994. Ecology Biol. Control 38:205-209. and Integrated Pest Management. Insect Sci. Tran, D.H., M. Takagi, and K. Takasu. 2005. Toxicity Appl. 6:557-582. of selective insecticides to Neochrysocharis van Lenteren, J.C., and J. Woets. 1988. Biological formosa (Westwood) (Hymenoptera: and integrated control in greenhouses. Annu. Eulophidae), a parasitoid of the American Rev. Entomol. 33:239-269. serpentine leafminer Liriomyza trifolii van Mele, P., and J.C. van Lenteren. 2002. Survey of (Burgess) (Diptera: Agrizomydae). J. Fac. current crop management practices in a mixed- Agric. Kyushu Univ. 50:109-118. ricefi eld landscape, Mekong Delta, Vietnam Urbaneja, A., E. Llácer, A. Garrido, and J. Jacas. potential of habitat manipulation for improved 2000. Indigenous Natural Enemies Associated control of citrus leafminer and citrus red mite. with Phyllocnistis citrella (Lepidoptera: Agr. Ecosys. Environ. 88:35-48. Gracillariidae) in Eastern Spain. Biol. Control Vercher, R., J. Costa-Comelles, C. Marzal, 18:199-207. and F. Garcia-Mari. 2005. Recruitment of Urbaneja, A., E. Llácer, A. Garrido, and J. Jacas. native parasitoid species by the invading 2001. Effect of variable photoperiod on leafminer Phyllocnistis citrella (Lepidoptera: development and survival of Cirrospilus Gracillariidae) on citrus in Spain. Environ. sp. nr. lyncus (Hymenoptera: Eulophidae), Entomol. 34:1129-1138. an ectoparasitoid of Phyllocnistis citrella Villanueva-Jiménez, J.A., and M.A. Hoy. 1998. (Lepidoptera:Gracillariidae). Fla. Entomol. Toxicity of pesticides to the citrus leafminer and 84:305-307. its parasitoid Ageniaspis citricola evaluated to 142 CIENCIA E INVESTIGACION AGRARIA

assess their suitability for an IPM program in of citrus leafminer, Phyllocnistis citrella citrus nurseries. BioControl 43:357-388. Stainton (Lepidoptera:Phyllocnistidae). Chin. Vincent, C., B. Rancourt, and O. Carisse. 2004. J. Entomol. 18:13-25. Apple leaf shredding as a non-chemical tool Xiao, Y., J.A. Qureshi, and P.A. Stansly. 2007. to manage apple scab and spotted tentiform Contribution of predation and parasitism to leafminer. Agr. Ecosys. Environ. 104:595-604. mortality of citrus leafminer Phyllocnistis Wang, L., M. You, J. Wang, and Q. Wu Q. 1999. citrella Stainton (Lepidoptera: Gracillariidae) Niches of citrus leafminer and its natural populations in Florida. Biol. Control 40:396- enemies. J. Fujian Agric. Univ. 28:319-324. 404. Weintraub, P.G. 1999. Effects of cyromazine Yarnes, C.T., and W.J. Boecklen. 2006. Abiotic and abamectin on the leafminer, Liriomyza mosaics affect seasonal variation of plant huidobrensis and its parasitoid, Diglyphus resources and infl uence the performance and isaea in celery Ann. Appl. Biol. 135:547-554. mortality of a leaf-miner in Gambel’s oak Weintraub, P.G., and A.R. Horowitz. 1998. (Quercus gambelii Nutt.). Ecol. Res. 21:157- Effects of translaminar versus conventional 163. insecticides on Liriomyza huidobrensis Yoder, J.A., and M.A. Hoy. 1998. Differences in (Diptera:Agromyzidae) and Diglyphus isaea water relations among the citrus leafminer (Hymenoptera:Eulophidae) populations in and two different populations of its parasitoid celery. J. Econ. Entomol. 91:1180-1185. inhabiting the same apparent microhabitat. West, S.A., J.M. Cook, J.H. Werren, and H.C.J. Entomol. Exp. Appl. 89:169-173. Godfray. 1998. Wolbachia in two insect hots- Zappala, L., and M.A. Hoy. 2004. Reproductive parasitoid communities. Mol. Ecol 7:1457- strategies and parasitization behavior of 1465. Ageniaspis citricola, a parasitoid of the citrus Wu T.K. and K.S. Lin. 1998. Infl uence of leafminer Phyllocnistis citrella. Entomol. Exp. green lacewing, Mallada basalis (Walker) Appl. 113:135-143. (Neuroptera:Chrysopidae), on parasitoids