Mass Production of Diglyphus Isaea

Entomological Research 47 (2017) 94–100

RESEARCH PAPER Mass production of Diglyphus isaea (Hymenoptera: Eulophidae), a biological control agent of a Korean population of potato leaf miner Liriomyza huidobrensis (Blanchard) (Diptera: Agromyzidae) Rameswor MAHARJAN1,2, Min KWON1,JuIlKIM1 and Chuleui JUNG3

1 Highland Agricultural Research Institute, National Institute of Crop Science, Pyeongchang, Rural Development Administration, Republic of Korea 2 Department of Southern Area Crop Science, National Institute of Crop Science, Miryang, Republic of Korea 3 Department of Plant Medicine, Andong National University, Andong, Republic of Korea

Correspondence Abstract Rameswor Maharjan, Highland Agricultural Research Institute, National Institute of Crop The potato leaf miner, Liriomyza huidobrensis (Blanchard), is an important pest of Science, 25342, Pyeongchang, Rural potato throughout the world, including Korea. A method was developed for mass Development Administration, Republic of rearing the parasitoid Diglyphus isaea (Walker) using faba bean, Vicia faba L. Korea. (Fabaceae), as the host-plant and L. huidobrensis as the insect host. Faba bean plants E-mail: [email protected] were planted in pots and maintained in a greenhouse for about 15 d. Pots were then exposed to adult leaf miners in oviposition cages for 4 h. Plants containing late Received 24 February 2016; accepted 10 October 2016. second to early third instar larvae were exposed to adult D. isaea in parasitoid cages for 24 h. The leaf area per pot after 15 d was 597.9 cm2, which produced 103.33 doi: 10.1111/1748-5967.12205 larvae per pot. The number of adult parasitoids emerging per pot was 72.5; about 41% of these were female. The daily cost of parasitoid production was USD20.95 per 1000 individual parasitoids. The methodology developed for D. isaea could be used to rear other ectoparasitoids such as Hemiptarsenus spp. and Pnigalio sp. with different insect hosts like L. trifolii. This is why this mass-rearing information is important for securing test insect materials for ecological and biological study of Liriomyza species, and also for developing a biological control for Liriomyza species other than L. huidobrensis by mass production of associated natural enemies. We are facing rapid agro-ecosystem changes including pest systems. Continuous monitoring of Liriomyza in solanaceous crops is needed.

Key words: biological control, Diglyphus, Liriomyza, mass rearing, relationships.

Introduction potato in Korea (Maharjan et al. 2014). Larvae of the leaf miner are polyphagous and cause both direct and indirect The genus Liriomyza (Diptera: Agromyzidae) includes 23 damage to plants (Musgrave et al. 1975; Minkenberg & Van species of economic importance because they damage a wide Lenteren 1986). Direct damage includes leaf puncturing, range of field and greenhouse crops and ornamental plants feeding and laying eggs in the leaf mesophyll (Weintraub & (Spencer 1973; Parrella 1987; Kang 1996; Cerny et al. Horowitz 1995). Larval feeding characteristics vary according 2001). Invasion is increasing in new areas worldwide to species, which can reduce photosynthesis by up to 62% (Minkenberg & Van Lenteren 1986; Weintraub & Horowitz (Johnson et al. 1983; Parrella et al. 1984; Heinz & Chaney 1995; Steck 1996). Nine species of Liriomyza are reported in 1995), accompanied by yield loss (Chandler & Gilstrap Korea (Ahn et al. 1994; Hong et al. 1996; Suh & Kwon 1987). Indirect damage includes vectoring for plant diseases 1998; Maharjan et al. 2014). Liriomyza huidobrensis has been (Alternaria alternate (Fr.) Keissl) (Zitter & Tsai 1977; recently noticed and considered as an emerging new pest in Matteoni & Broadbent 1988; Deadman et al. 2002).

Currently, chemical methods are the first options for It is common in Gangwon, north and south Chungcheon, controlling this invasive pest (Cox et al. 1995). north and south Gyeongsang and north and south Jeolla However, high reliance on insecticides had been followed provinces in mainland Korea (R Maharjan & C Jung, 2012). by the development of insecticide resistance and the This paper describes the mass production system of D. isaea subsequent reduction in natural enemy populations, which is using faba bean and potato leaf miner fly as a host-plant and exacerbated by improper management (Johnson et al. 1980a; insect host, respectively. Additionally, cost analysis of the Lange et al. 1980; Trumble 1981; Parrella et al. 1984; Chavez rearing protocol is provided. & Raman 1987; Mason & Johnson 1988; Sanderson et al. 1989; MacDonald 1991; Ferguson 2004). Thus, biological control by releasing a mass-produced biocontrol agent could Materials and methods be a sustainable and environmentally friendly option for this secondary pest in both protected cultivation (Parrella 1982) Plant production and open fields where additional control could be expected from natural enemies (Johnson & Hara 1987; Johnson 1993; Faba bean, Vicia feba (Fabaceae), was planted weekly in pots Liu et al. 2009). (18 cm diameter, 13 cm height) using commercial soil media Liriomyza leaf miner flies are known to have natural (Plant World, Gyeonggi, Korea); three to five plants were enemies (Waterhouse & Norris 1987; Murphy & LaSalle positioned in each pot. Plants were stored on greenhouse 1999). Parasitoids are the major group of natural enemies of benches and watered manually as needed. The plants were leaf miner flies (Parrella 1987; Kang 1996). Noyes (2004) kept for 10–15 d in greenhouse conditions (28 Æ 2°C, listed more than 80 species of parasitoid wasps that attack 50–70% relative humidity under conditions of 16 h light : 8 h various stages of Liriomyza species. Genus Diglyphus in the dark (LD 16:8)). Environmental conditions were recorded by family Eulopidae constitutes one of the most important using data loggers (Easy Log-WIN-USB, Garage, Essex, parasitoid groups of Liriomyza spp. (Johnson & Hara 1987; United Kingdom, Lascar Electronics UK-onset computer, Waterhouse & Norris 1987; Minkenberg 1990; Johnson Garage, Essex, United Kingdom). At this time plants were 1993; Liu et al. 2009; Cisneros & Mujica 1998; Mujica & about 30–40 cm tall, with sufficient leaves. Kroschel 2011). Successful control of leaf miner species Leaf area index would allow comparison between faba bean through migration of Diglyphus spp. has been reported in and other potential host-plants (i.e., Phaseolus spp.). Areas of Europe (Nedstam 1987, Nucifora & Vacante 1987). In 175 individual faba bean leaves (dependent variable) were California celery, Diglyphus spp. provided adequate control measured with a leaf area meter (CI-202; CID Inc., Camas, of L. trifolii (Burgess), as did pesticides (Trumble 1985). Washington, USA) and these were regressed on leaf length Inoculative–inundative release programs of Diglyphus spp. (independent variable) (SAS Institute 2009). This relationship have been reported in many countries especially to control was used to calculate total leaf area of each pot used in the L. trifolii in greenhouses (Gaviria et al. 1982; Lyon 1985; rearing study. Wardlow 1985; Woets 1985). Until now no information about mass-rearing of ectoparasitoids on a Korean population of Leaf miner production L. huidobrensis using faba bean has been documented in Korea. For oviposition, adult leaf miners were held in acrylic cages Diglyphus isaea is a primary parasitoid of Agromyzidae (40 cm height × 60 cm width × 80 cm length) with openings leaf miners (Sher et al. 1996; Zhu et al. 2000) and is in the sides covered with meshed screens for ventilation. considered as the most effective biocontrol agent of leaf miner Conditions in greenhouses were maintained under a flies including L. huidobrensis. Diglyphus isaea is a photoperiod of LD 16:8 and at temperatures between 21 and facultative gregarious parasitoid and the adult females lay 28°C. Relative humidity fluctuated between 40 and 70%. one to five eggs adjacent to late leaf miner larval stages. The Uniform numbers of leaf miners were maintained in these parasitoid larvae feed on the host for about 5 d then pupate cages by releasing a constant number (about 200, sex ratio in the mine. The adult parasitoids emerge after about 5.5 d of male : female of 1:1) of adults daily into the cage. This and live for about 10 d (Minkenberg & Fredrix 1989). action kept the population in each cage between 1000 and Morphological features such as cubital vein strongly curved 1500. Preliminary experiments revealed that the variance at base; speculum very narrow or absent; scutellum shiny associated with the mean number of parasitoids produced and violet; and all coxae, trochanter, basal 3/4 of femora, per pot stabilized with a sample size of at least six pots. Six and tibiae dark except for base or apical 1/5–1/6 distinguish potted faba beans were exposed in each cage for 4 h, usually D. isaea from all other species of Diglyphus (Gonzalez et al. between 07.00 and 11.00 h. This number of pots was chosen 1979; Zhu et al. 2000). Currently, D. isaea is considered as to assure a stable variance and for convenience because six a single species with a worldwide distribution (Noyes 2002). pots fit perfectly into a standard greenhouse flat

(approximately 2000 cm2). For the purposes of documenting so in total 18 pots were used to determine production statistics. leaf miner and parasitoid production per pot, three replicates On a per-pot basis, leaf area, number of newly hatched larvae, of six pots were monitored through the rearing process on number of larvae surviving exposure to the parasitoids and separate days. number of the parasitoids were calculated. The rearing A short exposure time to adult leaf miners assured that all procedure was divided into the following components: potting eggs were deposited in the plants at nearly the same time and maintaining plants, exposing pots to leaf miner, exposing and that larval development would be synchronous. Pots were pots to parasitoids, sand-filled trays, plant and leaf miner replaced on greenhouse benches after exposure; after 3 d, all colony maintenance while parasitoids developed, cutting newly hatched larvae were counted. When most larvae plants and placing in sleeve cages, and aspirating parasitoids reached the late second or early third instar (after from cages. Each of these categories was timed during approximately 3–5 d from egg hatching), they were ready parasitoid production over a 3–4-d period, and the time for exposure to the parasitoids. Plants to be used only for leaf required to produce 3000–4000 D. isaea per day was miner production were cut at the soil line and placed on calculated. screens over sand-filled trays to collect pupae. The sand was The cost of production was divided into nonrecurring costs passed through a fine screen to separate pupae. Counting the (e.g., cages and pots) and recurring costs (e.g., plants, soil and pupae was very tedious, so the relationship between the fertilizer) using prices from 2015. Cost of space (greenhouse weight of pupae (independent variable) and number of pupae rooms) and utilities was not included in the overall cost. (dependent variable) of 100 samples encompassing 37 to 160 pupae was determined by a linear regression model (LRM) (SAS Institute 2009). Statistical analysis Relationship between leaf area and leaf length, and pupa Parasitoid production number and pupa weight, were calculated by LRM (SAS Institute 2009). Adult D. isaea were held in acrylic cages (43 cm height × 80.5 cm weight × 60.2 cm length) with openings in the sides covered with meshed screens for ventilation. These cages were located in greenhouse rooms under conditions described Results previously for the leaf miner. Uniform numbers of parasitoids A significant relationship between leaf area and leaf length were maintained in these cages by adjusting the number was found (Reg. F = 513.81, df = 1173, P < 0.0001; released daily into each cage (approximately 50, sex ratio of R2 = 0.76) (Fig. 1). This relationship allowed rapid estimation male : female 1:1). These releases kept the population in each of leaf area per pot by the use of a nondestructive method cage at about 200–300. (measuring leaf length). After 15 d of plant growth, leaf area Six potted faba beans, each containing second or third per pot was 597.9 Æ 0.5 cm2. Exposing six pots for 4 h in instars, were exposed in each cage for 24 h. After exposure, cages with 1000 to 1500 adult flies resulted in 103.33 Æ 1.4 the pots were held horizontally for 2 d on tip-racks with newly hatched larvae per pot. Fewer than five larvae per leaf sand-filled trays. Leaf miner larvae that survived exposure to the parasitoid emerged and were collected in these trays. Plants were then moved to another greenhouse room for parasitoid development. After about 10 d (just before parasitoid emergence from leaves), plants were cut at the soil line and placed in glass-topped sleeve cages. As they emerged, parasites were collected in small vials with hand-held aspirators. Adult parasitoids were returned to cages for parasitoid production.

Analysis of the rearing protocol To document the rearing procedure, pots were held individually to determine the number of leaf miners that survived parasitoid exposure per pot and the number and sex of parasitoids per pot. As discussed previously, six pots were Figure 1 Regression analysis of faba bean leaf area vs. length (n =175 followed through the rearing procedure on three separate days, leaves) (Reg. F = 513.81, df = 1,173, P < 0.0001).

96 Entomological Research 47 (2017) 94–100 © 2017 The Entomological Society of Korea and John Wiley & Sons Australia, Ltd Rearing of parasitoids were usually present. So, intraspecific competition was not phototactic response), these methods must include some found to be a problem. mechanism for quantifying parasitoid production as well as Estimation of the number of leaf miner pupae was made for calculating the sex ratio. The latter two aspects take easier by the strong relationship with pupal weight considerable time. (R2 = 0.74) (Reg. F = 254.70, df = 1,98, P < 0.0001; The total cost of producing 4000 D. isaea was estimated to R2 = 0.74) (Fig. 2). This estimation method is often used for be USD4528.40 (Table 2). For this estimation, more time was leaf miner production. After exposure of pots to the parasitoid given labor (8 h) than was required (6.67 h, Table 2) to allow cage, 54.9 Æ 1.3 leaf miner larvae per pot survived and some flexibility in the timing for each procedure. When pupated in the sand-filled trays. These emerged and were production was underway, the only recurring costs that needed returned to the leaf miner colony cages as needed. Parasitoid to be considered were labor, soil and plants. Therefore, the production was 72.5 Æ 1.2 per pot; 41% of these were female. recurring cost of parasitoid production was USD83.80 per Production was equivalent to 0.12 parasitoids per square cm of 4000 parasitoids. This figure could underestimate the real faba bean leaf. costs because the costs and depreciation of greenhouse space, Approximately 398.4 min. was required to produce 4000 machinery and utilities were not taken into consideration. adult parasitoids (Table 1). More than 50% of this time was devoted to the tedious task of aspirating parasites into vials. Although other methods could be developed for Discussion parasitoid removal (e.g., anesthetization or use of the Faba bean is relatively fast growing compared with other hosts such as pumpkin and cucumber; approximately 15 d (in optimum condition) is required when a plant is suitable for parasitoid production (Table 1, Fig. 3). It is important to choose the right plant and insect host for rearing any insect and parasitoids. Salvo and Valladares (2002) reported that the size of Liriomyza leaf miner and its suitability for parasitoid varies with the plant host in both natural habitats and cultivated areas. The cost of faba bean and use of this plant in the rearing process would reduce the possible conditioning of the parasitoids to another host-plant. The use of the Korean population of L. huidobrensis as the host leaf miner, and rearing the parasitoids under general greenhouse conditions, mean that they will quickly acclimatization to the field environment, which should increase their potential parasitism. The size of parasitoids can be a useful character, although this Figure 2 Regression analysis of leaf miner pupa number versus pupa was not quantified. Charnov et al. (1981) showed the solitary weight (n = 100 samples) (Reg. F = 254.70, df = 1,98, P < 0.0001). parasitoid adult size is closely correlated with host size.

Table 1 Labor required per day in mass production of Diglyphus isaea using faba bean as a host-plant and Liriomyza huidobrensis as the insect host

Time†

Procedure Days Per pot (s)(mean Æ SE) Per 4000 parasitoids (min)

Potting and maintaining plants 1–20 53.8 Æ 1. 6 4 4. 5 Exposing plants to leaf miner 20 34.7 Æ 1. 6 2 8. 4 Exposing plants to parasitoids 25 56.2 Æ 0.7 46.3 Plants placed on tip racks 26 20.7 Æ 1. 0 17. 2 Plants and leaf miner colony maintenance while parasitoids develop 28 4.3 Æ 0.4 3.5 Cutting plants and place in cages 40 21.7 Æ 2.3 18.1 Aspirating parasitoids from cage 43 – 240.5 Total 398.4

†Based on three replicates of the entire process. For 4000 parasites, 50 pots are required with 80 parasites per pot. –, not calculated

Table 2 Cost estimates for the production of 4000 Diglyphus isaea per of the parasitoid D. isaea population would be higher when day using faba bean as the host-plant and Liriomyza huidobrensis as the produced from larger host insect species. The female insect host proportion in any D. isaea population in augmentative and mass rearing is important, because females are more important Quantity Unit cost (USD) Total cost (USD) as they are directly responsible for pest population regulation

Labor (Ode & Heinz 2002). In this rearing procedure, the female Technician (1 full time) 8 h 5.9 46.8 proportion was 41%, which was significantly lower than the Materials maximum values of 70–75% of Ode and Heinz (2002) and Nonrecurring costs Musundire et al. (2012). Production of D. isaea as a biological Pots 50 0.3 12.5 control agent is expensive, with a large and complex Aspirator 1 12.0 12.0 production system. For this reason, improvement of the Test tubes 7 0.8 5.6 female : male ratio in the population is an important quality Vials 20 0.6 12.0 management option. Ode and Heinz (2002) advocated the Vial holders 5 0.5 2.5 host–size-dependent sex ratio theory with high-quality, larger Analytical balance 1 1250.0 1250.0 size host insect production using agromizid leaf miners. Trays 10 7.0 70.0 Further, Musundire et al. (2012) described that Liriomyza Cages 12 90.0 1080.0 Tipping racks 4 350.0 1400.0 species and D. isaea can be used for further larger scale field Holding racks 4 150.0 600.0 studies aimed at optimizing field releases and adapting mass Recurring costs rearing of D. isaea on different plant species. Field-collected Soil mix 70 kg 1.3 21.0 populations are being added regularly for colony vigor. The Plants (seed) 150 0.10 16.0 cost of USD20.95 per 1000 parasitoids (recurring costs only) Total 4528.4 is much lower than current prices charged for leaf miner parasitoids in the Korean market. Some of the sources of D. isaea in Korea (e.g., Dongbu Ceres Co., Nonsan, Korea) currently charges USD44.00 for 250 parasitoids. By using Although host sizes of L. huidobrensis larvae were not our method or a modification if it, mass production of measured in this study, studies by Spencer (1973) and D. isaea in the greenhouse environment or even in the field Musundire et al. (2012) showed that under uniform could be possible, which could contribute to the biological conditions, L. huidobrensis larvae are larger than those of control of leaf miner flies. More vigorous testing of the L. sativae and L. trifolii, suggesting that this species should system could improve the productivity and quality leading receive a higher allocation of female progeny compared with to ecologically efficient and economically achievable larvae of L. sativae and L. trifolii. Thus the female proportion management of invasive Liriomyza pests.

Figure 3 Schematic of overall rearing procedures for D. isaea using faba bean as a host-plant and L. huidobrensis as the insect host. (Modification based on the training from International Potato Center (CIP), Lima, Peru). PLANTS FOR Liriomyza COLONY MAINTANCE; PLANTS FOR PRODUCTION OF Diglyphus; OVERNIGHT PLANTS FOR Liriomyza; *Liriomyza pupa; D ADULT Diglyphus

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