Acceptability and Suitability of Three Liriomyza Species as Host for the Endoparasitoid Halticoptera arduine (Hymenoptera: Pteromalidae)

Acceptability and Suitability of Three Liriomyza Species as Host for the Endoparasitoid... Abstract In the scope of using Halticoptera arduine (Walker; Hymenoptera: Pteromalidae) in a classical biological control program in East Africa, laboratory bioassays were conducted to evaluate the acceptability and suitability of the three economically important Liriomyza leafminer species to the exotic parasitoid. Searching time, number of oviposition attempts, F1 parasitoid developmental period, parasitism rates, sex ratio, host mortality, and body size indices were assessed. H. arduine parasitized and developed successfully in the three Liriomyza species reported in East Africa. Female parasitoids took on average between 10.45 ± 0.83 to 15.80 ± 0.91 (means ± SE) seconds to encounter their first host and made significantly more oviposition attempts on Liriomyza huidobrensis (Blanchard; Diptera: Agromyzidae) than Liriomyza sativae (Blanchard; Diptera: Agromyzidae) and Liriomyza trifolii (Burgess; Diptera: Agromyzidae) (P = 0.0006). Parasitoid development period from egg to adult ranged between 19.32 ± 0.96 and 22.86 ± 0.27 d. Parasitism rate ranged from 27.96 ± 3.86 to 44.10 ± 4.56 in the three host species and was significantly higher in L. huidobrensis than in L. sativae (P = 0.0397). H. arduine did not induce significant nonreproductive host mortality in any of the three Liriomyza hosts. A female-biased parasitoid sex ratio was observed in L. huidobrensis, a balanced sex ratio in L. sativae and a male-biased in L. trifolii. Parasitoids progeny were significantly larger on L. huidobrensis for both tibia and wing length than L. sativae and L. trifolii (P = 0.0109 and P = 0.0192, respectively). The implication for the environmentally friendly management of Liriomyza leafminers in East Africa is discussed. Leafminer flies, developmental period, parasitism, fitness, East Africa Liriomyza (Diptera: Agromyzidae), commonly referred to as Leafminer flies contains more than 300 species distributed worldwide (Spencer 1973, Liu et al. 2009, Mujica and Kroschel 2011). The genus is believed to be of Neotropic origin which had restricted distribution to the New World until the mid 1970s (Waterhouse and Norris 1987, Murphy and LaSalle, 1999). Twenty-three species are of economic importance causing damage to a wide range of horticultural and ornamental crops (Morgan et al. 2000, van der Linden 2004). Several species of the Liriomyza have since invaded new areas worldwide (Shepard et al. 1998, Rauf et al. 2000; Bjorksten et al. 2005). Liriomyza trifolii (Burgess; Diptera: Agromyzidae) was first reported in Kenya in 1976 through Chrysanthemum spp. (Asterales: Asteraceae) cuttings from Florida, United States, and was subsequently recorded in other localities from the coastal areas to the highlands (Spencer 1985). Three highly polyphagous leafminer fly species, Liriomyza huidobrensis (Blanchard; Diptera: Agromyzidae), Liriomyza sativae (Blanchard; Diptera: Agromyzidae), and L. trifolii (Burgess) (Diptera: Agromyzidae) are currently the predominant invasive species frequently reported from Kenya (Chabi-Olaye et al. 2008, Gitonga et al. 2010, Foba et al. 2015b). Adult female leafminers cause damage on leaves by puncturing using their ovipositor on which they feed from leaf exudates and insert eggs. Males are unable to puncture leaves but feed from punctures produced by females. The punctures may act as pathway for diseases vectors such as Alternaria alternata ((Fr.) Keissl; Pleosporales: Pleosporaceae) (Zitter and Tsai 1977, Parrella et al. 1984, Matteoni and Broadbent 1988, Deadman et al. 2002, Bjorksten et al. 2005). Larval mining of leaves is the most destructive feeding behavior and may lead to leaf fall in severe infestation, delay in plant development, and yield loss (Johnson et al. 1983, EPPO 2013). The larval stage is also difficult to control due to its concealed nature in plant tissues. Liriomyza species are categorization as quarantine pest (EC 2000, IPPC 2005, Anderson and Hofsvang 2010, EPPO 2013, EUROPHYT 2018) posing a trade barrier in fresh horticultural products. In Kenya, Liriomyza species attack a variety of horticultural commercial value crops including snow pea (Pisum sativum (L.; Fabales: Fabaceae)), French bean (Phaseolus vulgaris (L.; Fabales: Fabaceae)), runner bean (Phaseolus coccineus (L.; Fabales: Fabaceae)), tomato (Lycospersicon esculentum (Miller; Solanales: Solanaceae)), potato (Solanum tuberosum (L.; Solanales: Solanaceae)), Eryngium sp. (L.; Apiales: Apiaceae), Gypsophila sp. (L.; Caryophyllales: Caryophyllaceae), and Carthamus sp. (L.; Asterales: Asteraceae) cut flowers (Chabi-Olaye et al. 2008, KEPHIS 2014, Foba et al. 2015b, Guantai et al. 2015). Horticulture is an important sector of agriculture providing employment to millions of people and generating foreign currency (McCulloch and Ota 2002, NHP 2012, KHC 2015). It contributes on average 25.3% of Kenya’s Gross Domestic Product (GDP and earned the country $2 billion in 2013 (KNBS 2015, KFC 2014). Several pesticide including organophosphates, carbamates, pyrethroids, and triazines (cryomazine) have been identified and adversely used for Liriomyza leafminer control which if used exclusively could quickly generate resistance (Weintraub and Horowitz 1997, Price and Nagle 2002, Guantai et al. 2015). The indiscriminate use of insecticides is likely to be one of the reasons for the leafminer outbreaks in their invaded ranges with negative effects to their natural enemies (Murphy and LaSalle 1999, Gitonga et al. 2010). In recent years, pesticide residues above acceptable levels have become a technical trade to barrier in horticultural products in the European market (RASFF 2014). In their native ranges, natural enemies are important in regulating Liriomyza species populations (Shepard et al. 1998, Murphy and LaSalle 1999, Rauf et al. 2000, Mujica and Kroschel 2011). More than 300 species of parasitoids are associated with leafminers worldwide (Noyes 2003). In Peru, a complex of 63 parasitoid species is associated with Liriomyza leafminers causing high leafminer mortality of between 20 and 55% (Mujica and Kroschel 2011). In contrast, the diversity of existing Liriomyza parasitoids in East Africa field crops is low with parasitism rates below 6% (Chabi-Olaye et al. 2008). Parasitoids associated with Liriomyza leafminers mainly comprises of Diglyphus isaea (Walker), Neochrysocharis formosa (Westwood; Hymenoptera: Eulophidae)), Hemiptarsenus varicornis (Girault; Hymenoptera: Eulophidae), and Opius dissitus (Muesebeck; Hymenoptera: Braconidae), (Chabi-Olaye et al. 2008, Guantai et al. 2015, Foba et al. 2015c). In view of improving biological control of Liriomyza leafminers and further boosting the parasitism rates in East Africa, Halticoptera arduine (Walker; Hymenoptera: Pteromalidae) was imported from Peru into Kenya by the International Centre of Insect Physiology and Ecology (ICIPE), Nairobi, in collaboration with the International Potato Centre (CIP), under Leafminer IPM program. H. arduine is a larval endoparasitoid of Agromyzid leafminers which completes its development within the host. After parasitization, the host larva continues to develop into pupal stage until the adult parasitoid emerges from the host pupal case. Shortly after emergence, adult female parasitoids begin searching for leafminer larvae on leaf surfaces and on encounter, deposits up to three eggs in one host but only one offspring develops per host (Arellano and Redolfi 1989). Sex ratio of H. arduine is affected by host density and fertilization of females where unfertilized females produce only males (Kroschel et al. 2016). Low (<10°C) and high (>30°C) temperatures also affect the reproduction and development of H. arduine (Prudencio 2010). However, not much on H. arduine biology including its searching behavior, host specificity studies, or its use in classical biological control programs has been reported. In its native origins, H. arduine is adapted to a wide range of ecological areas efficiently parasitizing up to seven species of Agromyzid leafminer fly species in a range of 25 host plants causing up to 67% parasitism rates (Sanchez and Redolfi 1989, Neder de Romȃn 2000, Mujica and Kroschel 2011, Kroschel et al. 2016). The potential performance of the exotic parasitoid in controlling local Liriomyza species needed an evaluation before its consideration for a classical biological control program. This acceptability research will address the questions as to whether H. arduine will search and accept to oviposit in three local Liriomyza host species. The suitability studies will provide answers to the question on whether eggs will complete development within the hosts, parasitoid performance, and their fitness in these three host species. The objective of this study was therefore to evaluate the acceptability and suitability of H. arduine to three Liriomyza species found in Kenya before its consideration for introduction as a biological control agent. MATERIALS AND METHODS Plant Materials Fourteen-days-old potted plants of faba bean, Vicia faba (L.; Fabales: Fabaceae) and rose coco beans, P. vulgaris L. (Fabales: Fabaceae) were raised and supplied from screen house at the International Center of Insect Physiology and Ecology (ICIPE) Duduville campus in Kenya in conical plastic pots (5.5 cm diameter and 7.3 cm height) with five plants per pot. Insect Colonies Leafminer colonies Colonies of L. huidobrensis were initiated from field collections in Nyeri (0°21′S, 36°57′E, 2200 m.a.s.l) in Central Kenya highlands of Nyeri County and reared on V. faba. V. faba was chosen because it had been found as the best host plant for laboratory rearing and maintenance of L. huidobrensis (Videla et al. 2006, Chabi-Olaye et al. 2013). L. sativae and L. trifolii colonies were initiated from field collections in Kibwezi (02°15′S 37°49′E, 965 m.a.s.l), Makindu (02°16′S 37°48′E, 991 m.a.s.l) and Masongaleni (02°22′S 38°08′E, 714 m.a.s.l) in the Eastern low-lying counties of Kenya (Chabi-Olaye et al. 2013) and reared on rose coco beans. Musundire et al. (2012) and Okoth (2011) reported that L. sativae and L. trifolii preferred P. vulgaris compared to other tested host plants for oviposition and development and this led to the use of P. vulgaris as experimental host plant. The colonies were reared in Perspex cages (60 cm length × 60 width × 60 cm) (made at icipe, Nairobi, Kenya) under species-specific controlled temperatures and humidity that were optimum for their development (Okoth 2011, Musundire et al. 2012, Foba et al. 2015b) (25 ± 2°C and 55 ± 5% RH for L. huidobrensis and 27 ± 2°C and 55 ± 5% RH for L. sativae and L. trifolii). Adult leafminers were fed on 10% sugar solution for 2 d after emergence before exposure to host plants for experimental use. Halticoptera arduine colony Initial culture of H. arduine, a solitary endoparasitoid of Liriomyza leafminers, was obtained from the International Potato Center (CIP) in Peru, where they were maintained on L. huidobrensis. The parasitoid was maintained in the quarantine facility at ICIPE on L. huidobrensis at 25°C ± 1 and 55–60% RH for 12 generations after establishment before its experimental use. Newly emerged parasitoids were maintained on honey solution as source of food for 2 d before their exposure to the host insect larvae. Experimental procedure The first set of acceptability experiments were conducted separately from the second set of suitability experiments which were sequentially conducted after the acceptability experiments. The acceptability experiment study was conducted using methodology described by Chabi-Olaye et al. (2013) in the assessment of Phaedrotoma scabriventris (Nixon; Hymenoptera: Braconidae) acceptability to three Liriomyza species. Procedures described by Chabi-Olaye et al. (2013) were used for suitability studies with slight modifications. Chabi-Olaye et al. (2013) used excised plants with only two infested leaves and immersed in water in 10-ml glass vial and 10 female parasitoids per replicate. In the present study, however, 50 infested whole-potted plants (10 pots × 5 plants/pot) were held per Perspex cage and 50 2-d-old H. arduine adults (1 male: 2 females) were released per replicate. In host acceptance experiments, faba bean plants were exposed to 2-d-old adults of L. huidobrensis for 24 h for egg laying and maintained in a cage for 5 to 6 d to get a cohort of same age larvae. A two-leaved faba bean stem infested by between 10- and 15-s third larval stages of L. huidobrensis was excised above the soil base and inserted into a glass vial (30 ml) in upright position supported by moist cotton wool. The set up was placed in clear Perspex cage (15 × 15 × 20 cm) with the top and sides covered by fine insect netting (150 × 150 µm) for aeration in controlled environment (25°C ± 1 and 55–60% RH) using a thermostatic electric heater (Xpelair, United Kingdom) and humidifier. A 2-d-old naive mated female adult of H. arduine was introduced into the cage. The behavioral activities of the parasitoid on the infested plant (time spent on host searching and encounter and number of oviposition attempts) were directly recorded by visual observation for a 2-h period per replicate. After the 2-h period, the female parasitoid was removed and the larvae incubated (25°C ± 1 and 55–60% RH) in plastic Petri dish for 3 d to allow for pupae development. After 6 d, each individual pupa was incubated (25°C ± 1 and 55–60% RH) in gelatin capsule (2.20 cm height and 0.7 cm diameter) for 8 to 16 d until adult leafminer or parasitoid emergence. Under these experimental conditions, average developmental times were 14 and 25 d for leafminer and parasitoid, respectively. The number of female parasitoids with successful oviposition in each host was confirmed by emergence or recovery of a parasitoid. The experiment was replicated 40 times and the same experimental set up was repeated using L. sativae and L. trifolii on P. vulgaris. In our second experiment, 200 2-d-old L. huidobrensis (at the ratio of 1 male: 2 females) were exposed to 10 pots of 2-wk-old faba bean plants (five plants/pot) for 24-h in Perspex cages (30 × 30 × 45 cm) with two sides covered by fine insect netting (150 × 150 µm) for aeration. The exposure of L. huidobrensis was done in 10 cages, five of which received the parasitoid treatment and five represented control with no parasitoids. Infested plants were held for 5 to 6 d to allow the development of same age cohort of second–third larval stages of leafminer. A batch of 50 2-d-old adult H. arduine parasitoids (at the ratio of 1 male: 2 females) were released in the five Perspex cages containing the infested plants for 24-h before removal. The host larvae were held on the plants for 5 to 6 d for pupae development. Each pupa was capsulated and incubated (25°C ± 1 and 55–60% RH) in transparent gelatin capsules (2.20 cm height and 0.7 cm diameter) for adult leafminers and parasitoids emergence. The control allowed for assessment of leafminer natural mortality. The same methodology was repeated for L. sativae and L. trifolii hosts reared on P. vulgaris at different times. This experiment thus, consisted of three treatments and each of the treatment represented a Liriomyza host species replicated five times alongside with a control in a completely randomized design. In both experiments, the number of pupae, emerged leafminer adults and first generation parasitoids (F1 offspring), F1 parasitoids developmental period, and sex ratio were recorded. Pupae without exit holes and with unemerged insects were dissected under Leica EZ4D binocular microscope (Leica Microsystems Switzerland Ltd 2007; Glattbrugg, Switzerland; LAS EZ V 1.5.0 software (LEITZ, Glattbrugg, Switzerland)) following the methodology described by Heinz and Parrella (1990) to correct parasitism rate and nonreproductive host mortality. Nonreproductive host mortality was expressed as a percentage of unviable pupae over the total pupae in each treatment as described by Foba et al. (2015a). The right forewing and right hind tibia of 10 randomly selected male and female F1 parasitoids were detached from the point of contact with thorax and images taken using Leica EZ4D microscope camera (Leica Microsystems Switzerland Ltd 2007; LAS EZ V 1.5.0 software (LEITZ)). Wings and hind tibia were spread in 70% ethanol and the lengths measured at 35× magnification (Heinz and Parrella 1990, Honek 1993, Videla et al. 2006, Okoth et al. 2014). Data Analyses For each Liriomyza species, absolute numbers of F1 progeny males and females parasitoids and dead pupae were analyzed using Chi-square test in R version 3.0.2 statistical software (R Development Core Team 2013) to determine differences in sex ratio and significance level of nonreproductive mortalities. Count data on searching time, oviposition attempts, developmental time, and number of parasitoids in a progeny and percentage data on parasitism rates, sex ratios, and mortalities were log and arcsine transformed, respectively, before being subjected to one-way analysis of variance. Where there was significant difference between Liriomyza species in regards to time taken for a female parasitoid to first encounter host, oviposition attempts made on larval hosts in a 2-h observation period, proportion of female parasitoids that successfully oviposited in the hosts, number of parasitoids in F1 progeny from each host, developmental time of F1 parasitoids, parasitism rates, pupal mortality, and body size indices, means were separated using Tukey–Kramer honest significant difference test (P < 0.05) (SAS 2013, JMP V11, 2013). Results Host Acceptance Results of H. arduine acceptability to Liriomyza host species after 2 h are presented in Table 1. The parasitoid accepted and successfully deposited eggs in the three Liriomyza species, with up to 97.50 ± 2.50 (means ± SE) % of females laying eggs in L. sativae and L. trifolii. The number of oviposition attempts per female within 2-h observation period were also high, ranging from 57.30 ± 2.06 to 66.20 ± 3.48, with a significantly higher number of oviposition attempts on L. huidobrensis compared to L. sativae and L. trifolii (F2,117 = 4.07, P = 0.0196). Females parasitoids took a short period of time (as low as 10.45 ± 0.83 to 13.30 ± 1.37 s) to search and encounter their first host for oviposition with significantly shorter time (F2,117 = 7.98, P = 0.0006) spent on L. trifolii than on L. sativae. However, searching and encountering time on L. huidobrensis was not significantly different from that observed on L. sativae and L. trifolii. Significantly more females parasitoids successfully oviposited in L. sativae and L. trifolii than in L. huidobrensis (F2,117 = 14.91, P < 0.0001) (Table 1). Table 1. Acceptability parameters of three Liriomyza species to Halticoptera arduine (mean ± SE) under laboratory conditions (25°C ± 1 and 55–60% RH) Variable indicator Liriomyza huidobrensis Liriomyza sativae Liriomyza trifolii Time taken (s) to search and encounter first host 13.30 ± 1.37ab 15.80 ± 0.91a 10.45 ± 0.83b Mean number of oviposition attempts per female parasitoid 66.20 ± 3.48a 57.38 ± 1.73b 57.30 ± 2.06b Proportion of female parasitoids with successful oviposition (%) 65.00 ± 7.64b 97.50 ± 2.50a 97.50 ± 2.50a Variable indicator Liriomyza huidobrensis Liriomyza sativae Liriomyza trifolii Time taken (s) to search and encounter first host 13.30 ± 1.37ab 15.80 ± 0.91a 10.45 ± 0.83b Mean number of oviposition attempts per female parasitoid 66.20 ± 3.48a 57.38 ± 1.73b 57.30 ± 2.06b Proportion of female parasitoids with successful oviposition (%) 65.00 ± 7.64b 97.50 ± 2.50a 97.50 ± 2.50a (s)- second, within row, means followed by the same letter are not significantly different at P ≤ 0.05 (Tukey–Kramer test). View Large Table 1. Acceptability parameters of three Liriomyza species to Halticoptera arduine (mean ± SE) under laboratory conditions (25°C ± 1 and 55–60% RH) Variable indicator Liriomyza huidobrensis Liriomyza sativae Liriomyza trifolii Time taken (s) to search and encounter first host 13.30 ± 1.37ab 15.80 ± 0.91a 10.45 ± 0.83b Mean number of oviposition attempts per female parasitoid 66.20 ± 3.48a 57.38 ± 1.73b 57.30 ± 2.06b Proportion of female parasitoids with successful oviposition (%) 65.00 ± 7.64b 97.50 ± 2.50a 97.50 ± 2.50a Variable indicator Liriomyza huidobrensis Liriomyza sativae Liriomyza trifolii Time taken (s) to search and encounter first host 13.30 ± 1.37ab 15.80 ± 0.91a 10.45 ± 0.83b Mean number of oviposition attempts per female parasitoid 66.20 ± 3.48a 57.38 ± 1.73b 57.30 ± 2.06b Proportion of female parasitoids with successful oviposition (%) 65.00 ± 7.64b 97.50 ± 2.50a 97.50 ± 2.50a (s)- second, within row, means followed by the same letter are not significantly different at P ≤ 0.05 (Tukey–Kramer test). View Large Host Suitability The three Liriomyza hosts tested were found suitable for H. arduine. The parasitoid took between 19.32 ± 0.96 and 22.86 ± 0.27 d to complete development from egg to adult in the three hosts. H. arduine parasitized significantly more L. huidobrensis than L. sativae (F2,12 = 4.05, P = 0.0452); however, the parasitism in L. trifolii was similar to the two other hosts (Table 2). Liriomyza hosts affected sex ratio of H. arduine F1 progeny with a significant female-biased sex ratio when reared on L. huidobrensis (χ2 = 18.84, P < 0.0001) compared to a balanced sex ratio when reared on L. sativae (χ2 = 0.00, P = 1.00) and a male biased when reared on L. trifolii (χ2 = 18.84, P < 0.0001). Across the treatments, the proportion of female parasitoids’ in F1 were not significantly different (F2,79 = 4.67, P = 0.4798) (Table 2). Table 2. Host suitability—effect of Liriomyza host species on Halticoptera arduine developmental time, parasitism rate, and sex ratio (mean ± SE) under laboratory conditions (25°C ± 1 and 55–60% RH) Variable indicator Liriomyza huidobrensis Liriomyza sativae Liriomyza trifolii F1 developmental time (d) 19.32 ± 0.96c 21.23 ± 0.16b 22.86 ± 0.27a Parasitism rate (%) 44.10 ± 4.56a 27.96 ± 3.86b 32.28 ± 3.65ab Proportion of female parasitoids in F1 progeny (%) 57.94 ± 9.32aA 49.32 ± 5.59aA 45.31 ± 6.43aB Proportion of male parasitoids in F1 progeny (%) 42.03 ± 9.32aB 50.68 ± 5.59aA 54.69 ± 6.43aA Mean number of parasitoids in F1 progeny 33.0 ± 5.11b 61.80 ± 2.15a 61.00 ± 4.83a Variable indicator Liriomyza huidobrensis Liriomyza sativae Liriomyza trifolii F1 developmental time (d) 19.32 ± 0.96c 21.23 ± 0.16b 22.86 ± 0.27a Parasitism rate (%) 44.10 ± 4.56a 27.96 ± 3.86b 32.28 ± 3.65ab Proportion of female parasitoids in F1 progeny (%) 57.94 ± 9.32aA 49.32 ± 5.59aA 45.31 ± 6.43aB Proportion of male parasitoids in F1 progeny (%) 42.03 ± 9.32aB 50.68 ± 5.59aA 54.69 ± 6.43aA Mean number of parasitoids in F1 progeny 33.0 ± 5.11b 61.80 ± 2.15a 61.00 ± 4.83a (d)-days, within row and for the same variable, means followed by the same lower case letter are not significantly different at P ≤ 0.05 (Tukey–Kramer test). For each Liriomyza species, means followed by same upper case letter for male and female are not significantly different at P ≤ 0.05 (Chi-square test). View Large Table 2. Host suitability—effect of Liriomyza host species on Halticoptera arduine developmental time, parasitism rate, and sex ratio (mean ± SE) under laboratory conditions (25°C ± 1 and 55–60% RH) Variable indicator Liriomyza huidobrensis Liriomyza sativae Liriomyza trifolii F1 developmental time (d) 19.32 ± 0.96c 21.23 ± 0.16b 22.86 ± 0.27a Parasitism rate (%) 44.10 ± 4.56a 27.96 ± 3.86b 32.28 ± 3.65ab Proportion of female parasitoids in F1 progeny (%) 57.94 ± 9.32aA 49.32 ± 5.59aA 45.31 ± 6.43aB Proportion of male parasitoids in F1 progeny (%) 42.03 ± 9.32aB 50.68 ± 5.59aA 54.69 ± 6.43aA Mean number of parasitoids in F1 progeny 33.0 ± 5.11b 61.80 ± 2.15a 61.00 ± 4.83a Variable indicator Liriomyza huidobrensis Liriomyza sativae Liriomyza trifolii F1 developmental time (d) 19.32 ± 0.96c 21.23 ± 0.16b 22.86 ± 0.27a Parasitism rate (%) 44.10 ± 4.56a 27.96 ± 3.86b 32.28 ± 3.65ab Proportion of female parasitoids in F1 progeny (%) 57.94 ± 9.32aA 49.32 ± 5.59aA 45.31 ± 6.43aB Proportion of male parasitoids in F1 progeny (%) 42.03 ± 9.32aB 50.68 ± 5.59aA 54.69 ± 6.43aA Mean number of parasitoids in F1 progeny 33.0 ± 5.11b 61.80 ± 2.15a 61.00 ± 4.83a (d)-days, within row and for the same variable, means followed by the same lower case letter are not significantly different at P ≤ 0.05 (Tukey–Kramer test). For each Liriomyza species, means followed by same upper case letter for male and female are not significantly different at P ≤ 0.05 (Chi-square test). View Large In the three Liriomyza hosts studied, H. arduine did not induce any significantly different nonreproductive host mortality in three hosts from the control (PLh = 0.0639, PLs = 0.2345, and PLt = 0.6155) (Table 3). Table 3. Host suitability—nonreproductive host mortality by Halticoptera arduine in three Liriomyza host species (means ± SE) under laboratory conditions (25°C ± 1 and 55–60% RH) Liriomyza huidobrensis Liriomyza sativae Liriomyza trifolii Host mortality in presence of parasitoids (%) 50.55 ± 4.58Aa 37.32 ± 2.97Aa 40.81 ± 2.36Aa Natural host mortality in control (%) 33.32 ± 2.99Aa 41.77 ± 2.17Aa 39.40 ± 1.98Aa χ2 3.43 1.41 0.25 P value 0.0639 0.2345 0.6155 Liriomyza huidobrensis Liriomyza sativae Liriomyza trifolii Host mortality in presence of parasitoids (%) 50.55 ± 4.58Aa 37.32 ± 2.97Aa 40.81 ± 2.36Aa Natural host mortality in control (%) 33.32 ± 2.99Aa 41.77 ± 2.17Aa 39.40 ± 1.98Aa χ2 3.43 1.41 0.25 P value 0.0639 0.2345 0.6155 Within rows (columns), means followed by the same lower (upper) case letter are not significantly different at P ≤ 0.05 (Tukey–Kramer) and (Chi-square) test in that respect. View Large Table 3. Host suitability—nonreproductive host mortality by Halticoptera arduine in three Liriomyza host species (means ± SE) under laboratory conditions (25°C ± 1 and 55–60% RH) Liriomyza huidobrensis Liriomyza sativae Liriomyza trifolii Host mortality in presence of parasitoids (%) 50.55 ± 4.58Aa 37.32 ± 2.97Aa 40.81 ± 2.36Aa Natural host mortality in control (%) 33.32 ± 2.99Aa 41.77 ± 2.17Aa 39.40 ± 1.98Aa χ2 3.43 1.41 0.25 P value 0.0639 0.2345 0.6155 Liriomyza huidobrensis Liriomyza sativae Liriomyza trifolii Host mortality in presence of parasitoids (%) 50.55 ± 4.58Aa 37.32 ± 2.97Aa 40.81 ± 2.36Aa Natural host mortality in control (%) 33.32 ± 2.99Aa 41.77 ± 2.17Aa 39.40 ± 1.98Aa χ2 3.43 1.41 0.25 P value 0.0639 0.2345 0.6155 Within rows (columns), means followed by the same lower (upper) case letter are not significantly different at P ≤ 0.05 (Tukey–Kramer) and (Chi-square) test in that respect. View Large Parasitoid fitness on the various Liriomyza hosts in F1 offspring are presented in Table 4. The forewing of H. arduine measured between 1.27 ± 0.04 and 1.43 ± 0.10 mm for the females and 1.19 ± 0.03 to 1.34 ± 0.02 mm for the males. The hind tibia length of the female parasitoids measured between 0.35 ± 0.01 and 0.40 ± 0.01 while that in the males measured between 0.34 ± 0.01 and 0.41 ± 0.02. Female parasitoids reared on L. huidobrensis had significantly longer forewing than those reared on L. trifolii while those of L. sativae did not significantly differ from either of the two hosts (F2,27 = 4.59, P = 0.0192). Similarly, female parasitoids reared on L. huidobrensis had significantly longer hind tibia than those reared on L. sativae and L. trifolii (F2,27 = 5.37, P = 0.0109) (Table 4). On the other hand, male parasitoids reared on L. trifolii and L. huidobrensis, had significantly longer forewing than those reared on L. sativae (F2,27 = 7.94, P = 0.0019) while their hind tibia were significantly longer for those reared on L. trifolii than from L. sativae. Hind tibia from L. huidobrensis were not significantly different from the two former hosts (F2,27 = 7.14, P = 0.0032). There was no significance difference in parasitoid wing and tibia lengths between male and females within host (L. huidobrensis: χ2 = 0.01, P = 0.9137 and χ2 = 0, P = 1; L. sativae: χ2 = 0.05, P = 0.8316 and χ2 = 0, P = 1; L. trifolii: χ2 = 0.0.01, P = 0.9294 and χ2 = 0, P = 1, respectively) (Table 4). Table 4. Host suitability—effect of Liriomyza host species on adult Halticoptera arduine fitness (means ± SE) under laboratory conditions (25°C ± 1 and 55–60% RH) Parasitoid body size indices Liriomyza huidobrensis Liriomyza sativae Liriomyza trifolii Forewing length (mm)  Females 1.43 ± 0.03aA 1.37 ± 0.04abA 1.27 ± 0.04bA  Males 1.29 ± 0.03aA 1.19 ± 0.03bA 1.34 ± 0.02aA  χ2 0.0118 0.0452 0.0079  P value 0.9137 0.8316 0.9294 Hind tibia length (mm)  Females 0.40 ± 0.01aA 0.36 ± 0.01bA 0.35 ± 0.01bA  Males 0.37 ± 0.01abA 0.34 ± 0.01bA 0.41 ± 0.02aA  χ2 0 0 0  P value 1 1 1 Parasitoid body size indices Liriomyza huidobrensis Liriomyza sativae Liriomyza trifolii Forewing length (mm)  Females 1.43 ± 0.03aA 1.37 ± 0.04abA 1.27 ± 0.04bA  Males 1.29 ± 0.03aA 1.19 ± 0.03bA 1.34 ± 0.02aA  χ2 0.0118 0.0452 0.0079  P value 0.9137 0.8316 0.9294 Hind tibia length (mm)  Females 0.40 ± 0.01aA 0.36 ± 0.01bA 0.35 ± 0.01bA  Males 0.37 ± 0.01abA 0.34 ± 0.01bA 0.41 ± 0.02aA  χ2 0 0 0  P value 1 1 1 Within rows (columns and for each parameter), means followed by the same lower (upper) case letter are not significantly different at P ≤ 0.05 according to Tukey–Kramer (Chi-square) test. View Large Table 4. Host suitability—effect of Liriomyza host species on adult Halticoptera arduine fitness (means ± SE) under laboratory conditions (25°C ± 1 and 55–60% RH) Parasitoid body size indices Liriomyza huidobrensis Liriomyza sativae Liriomyza trifolii Forewing length (mm)  Females 1.43 ± 0.03aA 1.37 ± 0.04abA 1.27 ± 0.04bA  Males 1.29 ± 0.03aA 1.19 ± 0.03bA 1.34 ± 0.02aA  χ2 0.0118 0.0452 0.0079  P value 0.9137 0.8316 0.9294 Hind tibia length (mm)  Females 0.40 ± 0.01aA 0.36 ± 0.01bA 0.35 ± 0.01bA  Males 0.37 ± 0.01abA 0.34 ± 0.01bA 0.41 ± 0.02aA  χ2 0 0 0  P value 1 1 1 Parasitoid body size indices Liriomyza huidobrensis Liriomyza sativae Liriomyza trifolii Forewing length (mm)  Females 1.43 ± 0.03aA 1.37 ± 0.04abA 1.27 ± 0.04bA  Males 1.29 ± 0.03aA 1.19 ± 0.03bA 1.34 ± 0.02aA  χ2 0.0118 0.0452 0.0079  P value 0.9137 0.8316 0.9294 Hind tibia length (mm)  Females 0.40 ± 0.01aA 0.36 ± 0.01bA 0.35 ± 0.01bA  Males 0.37 ± 0.01abA 0.34 ± 0.01bA 0.41 ± 0.02aA  χ2 0 0 0  P value 1 1 1 Within rows (columns and for each parameter), means followed by the same lower (upper) case letter are not significantly different at P ≤ 0.05 according to Tukey–Kramer (Chi-square) test. View Large Discussion Parasitoids spend a significant amount of time searching for hosts, while a significant amount of time is spent probing the host to assess their suitability before making the decision to oviposit. The success of parasitoid–host relationship assumes a hierarchy of discrete steps that include habitat location, host location, host acceptance, host suitability (Doutt 1959, Vinson 1976), and host regulation (Vinson and Iwantsch 1980). Vinson (1975) considered host acceptance as the most important step for parasitoid success. H. arduine, the exotic endoparasitoid of Liriomyza leafminer accepted to oviposit and developed successfully in the three common Liriomyza hosts found in Kenya. Previous studies on the searching behavior of H. arduine showed that females encountered L. huidobrensis larvae immediately on their introduction to V. faba infested plants (Prudencio 2010). This concurs with our observations on the three Liriomyza hosts. Plant physical and chemical characteristics have an effect on searching time, movement, and foraging success of parasitoids (Andow and Prokrym 1990, Lukianchuk and Smith 1997, Lovinger et al. 2000, Suverkropp et al. 2001, Wang and Keller 2002). However, H. arduine searching behavior seemed not to be affected by host plant. Searching time on L. huidobrensis reared on V. faba was not different from the one on L. sativae and L. trifolii, both reared on P. vulgaris. The significant difference was rather between L. sativae and L. trifolii despite both being reared on the same plant. We, therefore, hypothesize that pest–host interaction could have influenced the searching behavior of H. arduine and thus recommend further studies to elucidate potential difference in chemical profile resulting from infestation of P. vulgaris by L. trifolii. Oviposition attempt by female parasitoids is considered as an important behavioral measurement for parasitoid host acceptance (Agboka et al. 2002). Considering the number of oviposition attempts made by H. arduine female on each of the Liriomyza hosts as selection decision for oviposition, it is evident that L. huidobrensis was a better choice for oviposition than L. sativae and L. trifolii, which also translated to a high parasitism rate on this host. Among the factors which influence the success of parasitoid development is the stage or instar at parasitization (Hegazi and Khafagi 2005). H. arduine prefers late second and early third larval instars of Liriomyza hosts for oviposition and parasitization (Arellano and Redolfi 1989) during which development to adult takes place. Results from this study showed that H. arduine completed its development within the three Liriomyza host species and our results were similar to that reported by Prudencio (2010) when reared on L. huidobrensis. This implies that H. arduine will successfully develop in the existing Liriomyza species occurring in Kenya’s agro-ecological systems and contribute to their natural control. However, further studies are required to assess its potential competition, complementarities or coexistence with indigenous parasitoids already present in the system. Various indigenous and exotic leafminer parasitoids have been reported in Kenya and this include mainly D. isaea, O. dissitus, and P. scabriventris which represent 95.18% of total parasitoids recorded at low, mid, and high altitudes of Kenya (Foba et al. 2015c). Male parasitoids only mate and do not contribute to pest mortality (Hassel et al. 1983, Comins and Wellings 1985). Male-biased populations of H. arduine have been reported by Arellano and Redolfi (1989), Neder de Romȃn (2000), and Prudencio (2010) when H. arduine was reared on low host population of L. huidobrensis and from lower and higher temperature developmental thresholds. The reverse was true when H. arduine was reared in high population of L. huidobrensis. (Neder de Romȃn, 2000). In contrast to these findings, our study revealed a female-biased and balanced sex ratio in L. huidobrensis and L. sativae hosts, respectively. In parasitoids, a balanced or female-biased sex ratio infers stability and higher efficiency compared to a male-biased one, as only females directly contribute to the mortality of pests (Beddington et al. 1978, Mills and Getz 1996, Ode and Heinz 2002, Pascua and Pascua 2004, Chow and Heinz 2005, Abe and Kamimura 2012, Foba et al. 2015a). Our results, therefore, suggest better reproduction potential for H. arduine in regards to the local populations of L. huidobrensis, L. sativae, and L. trifolii in Kenya. With insects, there is generally a positive relationship between body size and performance (Clutton-Brock 1988, Honek 1993) and fitness (Stoepler et al. 2011). The success of parasitoid to develop and complete its life cycle in a suitable host is influenced by other factors, host size (Lawrence 1990) which positively correlates with adult parasitoid size (Spencer 1990, Visser 1994, Lampson et al. 1996, Fidgen et al. 2000, Roitberg et al. 2001, Teder and Tammaru 2002). Additionally, performance of Agromyzid leafminer parasitoids depends on the body size of their hosts (Heinz and Parrella 1990, Spencer 1990, Salvo and Valladares, 1995, Ode and Heinz, 2002). However, host size is not necessarily the only indicator of parasitoid performance and other factors such as host plants can influence parasitoid performance (Salvo and Valladares 2002, Tran et al. 2007, Musundire et al. 2010). In our present studies, H. arduine female progeny reared on L. huidobrensis were larger than those reared on L. sativae and L. trifolii. In similar studies, Neochrysocahris okazakii (Kamijo; Hymenoptera: Eulophidae) reared on Liriomyza chinensis (Kato; Diptera: Agromyzidae) were larger than those reared on L. trifolii (Tran and Takagi 2005, Tran et al. 2007). Similarly P. scabriventris reared on L. huidobrensis were found to be larger than those reared on L. sativae and L. trifolii (Chabi-Olaye et al. 2013). It is assumed that larger hosts represent greater resource quantity for parasitoid development (Charnov 1982, Charnov and Skinner 1985) and performance (fecundity) (Musundire et al. 2012) with greater longevity, better searching capacity, and higher dispersal ability (Godfray 1994, Visser 1994). Studies by Spencer (1973) and Musundire et al. (2012) have confirmed that L. huidobrensis is larger in body size than L. sativae and L. trifolii. This suggests that the body size of the host affected the fitness of the parasitoid in the present study. Nonreproductive host mortality caused by parasitoids has been reported to constitute an important component in pest suppression in many studies (Sandlan 1979, Walter 1988, Tran and Takagi 2006, Bernardo et al. 2006, Akutse et al. 2015). However, this is more commonly reported among ectoparasitoids than in endoparasitoids. For example, Mafi and Ohbayashi (2010) observed that Sympiesis striatipes (Ashmead; Hymenoptera: Eulophidae) an ectoparasitoid, caused nonreproductive mortality of 44.7 ± 4.2% on citrus leafminer, Phyllocnistis citrella (Stainton; Lepidoptera: Gracillariidae). Similarly, female wasps of D. isaea were reported to cause significant nonreproductive mortality of Liriomyza larvae by host feeding and stinging without oviposition (Minkenberg 1989, Liu et al. 2013, Akutse et al. 2015). Copidosoma koehleri (Blanchard; Hymenoptera: Encyrtidae), an egg-larval endoparasitoid of potato tuber moth Phthorimaea operculella (Zeller; Lepidoptera: Gelechiidae) is one of the few exceptions of endoparasitoids reported to cause nonreproductive mortality (Keinan et al. 2012). In the present study, no significant nonreproductive host mortalities were recorded in H. arduine in any of the three host’s studies. These results concur with the findings of Prudencio (2010) who reported nonreproductive mortalities as low as 7% in H. arduine when reared on L. huidobrensis. Similar findings of such poor endoparasitoid-induced nonreproductive host mortality in Liriomyza leafminer were reported by Chabi-Olaye et al. (2013) and Foba et al. (2015a) while studying the performance of P. scabriventris against L. huidobrensis. In conclusion, this study has established that H. arduine can accept to oviposit and develop successfully in the three most economically important Liriomyza leafminers in East Africa and was not affected by host plant. The performance of the parasitoid should also be mainly based on its parasitism potential since it caused no significant nonreproductive mortality in the hosts. Parasitism rates, fitness, and sex-ratio parameters of the parasitoid were all promising. Considering that the three Liriomyza leafminer species studied are the most important across Africa, we hypothesize that H. arduine can successfully establish and contribute to the control of Liriomyza leafminers in Africa in general and particularly in Kenya. Pilot sites and open-field release activities are warranted to test and confirm this hypothesis. However, prior to this, to ensure that local parasitoid populations are not displaced by the exotic species, interaction studies between H. arduine and the parasitoids already existing in the system are warranted. Acknowledgments The authors are grateful to Jürgen Kroschel and Norman Mujica of the International Potato Center (CIP) in Peru for providing H. arduine specimens to start the colony in Kenya. The first author was supported through the Dissertation and Research Internship Program (DRIP) of icipe. The present study was conducted with financial support from the German Federal Ministry for Economic Cooperation and Development (BMZ) (Grant number: 09.7860.1-001.00; Contract number: 81121261). We are also grateful to UK Aid of the UK Government, the Swedish International Development Cooperation Agency (Sida), the Swiss Agency for Development and Cooperation (SDC), and the Kenyan Government for their core support to icipe that facilitated the present work. 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Activity patterns and egg production in Coccophagus bartletti, an aphelinid parasitoid of scale insects . Ecol. Entomol . 13 : 95 – 105 . Google Scholar CrossRef Search ADS Zitter , T. A. , and J. H. Tsai . 1977 . Transmission of three potyviruses by the leafminer Liriomyza sativae (Diptera: Agromyzidae) . Plant. Dis. Rep . 61 : 1025 – 1029 . © The Author(s) 2018. Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Environmental Entomology Oxford University Press

Acceptability and Suitability of Three Liriomyza Species as Host for the Endoparasitoid Halticoptera arduine (Hymenoptera: Pteromalidae)

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Entomological Society of America
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© The Author(s) 2018. Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
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0046-225X
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1938-2936
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10.1093/ee/nvy050
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Abstract

Abstract In the scope of using Halticoptera arduine (Walker; Hymenoptera: Pteromalidae) in a classical biological control program in East Africa, laboratory bioassays were conducted to evaluate the acceptability and suitability of the three economically important Liriomyza leafminer species to the exotic parasitoid. Searching time, number of oviposition attempts, F1 parasitoid developmental period, parasitism rates, sex ratio, host mortality, and body size indices were assessed. H. arduine parasitized and developed successfully in the three Liriomyza species reported in East Africa. Female parasitoids took on average between 10.45 ± 0.83 to 15.80 ± 0.91 (means ± SE) seconds to encounter their first host and made significantly more oviposition attempts on Liriomyza huidobrensis (Blanchard; Diptera: Agromyzidae) than Liriomyza sativae (Blanchard; Diptera: Agromyzidae) and Liriomyza trifolii (Burgess; Diptera: Agromyzidae) (P = 0.0006). Parasitoid development period from egg to adult ranged between 19.32 ± 0.96 and 22.86 ± 0.27 d. Parasitism rate ranged from 27.96 ± 3.86 to 44.10 ± 4.56 in the three host species and was significantly higher in L. huidobrensis than in L. sativae (P = 0.0397). H. arduine did not induce significant nonreproductive host mortality in any of the three Liriomyza hosts. A female-biased parasitoid sex ratio was observed in L. huidobrensis, a balanced sex ratio in L. sativae and a male-biased in L. trifolii. Parasitoids progeny were significantly larger on L. huidobrensis for both tibia and wing length than L. sativae and L. trifolii (P = 0.0109 and P = 0.0192, respectively). The implication for the environmentally friendly management of Liriomyza leafminers in East Africa is discussed. Leafminer flies, developmental period, parasitism, fitness, East Africa Liriomyza (Diptera: Agromyzidae), commonly referred to as Leafminer flies contains more than 300 species distributed worldwide (Spencer 1973, Liu et al. 2009, Mujica and Kroschel 2011). The genus is believed to be of Neotropic origin which had restricted distribution to the New World until the mid 1970s (Waterhouse and Norris 1987, Murphy and LaSalle, 1999). Twenty-three species are of economic importance causing damage to a wide range of horticultural and ornamental crops (Morgan et al. 2000, van der Linden 2004). Several species of the Liriomyza have since invaded new areas worldwide (Shepard et al. 1998, Rauf et al. 2000; Bjorksten et al. 2005). Liriomyza trifolii (Burgess; Diptera: Agromyzidae) was first reported in Kenya in 1976 through Chrysanthemum spp. (Asterales: Asteraceae) cuttings from Florida, United States, and was subsequently recorded in other localities from the coastal areas to the highlands (Spencer 1985). Three highly polyphagous leafminer fly species, Liriomyza huidobrensis (Blanchard; Diptera: Agromyzidae), Liriomyza sativae (Blanchard; Diptera: Agromyzidae), and L. trifolii (Burgess) (Diptera: Agromyzidae) are currently the predominant invasive species frequently reported from Kenya (Chabi-Olaye et al. 2008, Gitonga et al. 2010, Foba et al. 2015b). Adult female leafminers cause damage on leaves by puncturing using their ovipositor on which they feed from leaf exudates and insert eggs. Males are unable to puncture leaves but feed from punctures produced by females. The punctures may act as pathway for diseases vectors such as Alternaria alternata ((Fr.) Keissl; Pleosporales: Pleosporaceae) (Zitter and Tsai 1977, Parrella et al. 1984, Matteoni and Broadbent 1988, Deadman et al. 2002, Bjorksten et al. 2005). Larval mining of leaves is the most destructive feeding behavior and may lead to leaf fall in severe infestation, delay in plant development, and yield loss (Johnson et al. 1983, EPPO 2013). The larval stage is also difficult to control due to its concealed nature in plant tissues. Liriomyza species are categorization as quarantine pest (EC 2000, IPPC 2005, Anderson and Hofsvang 2010, EPPO 2013, EUROPHYT 2018) posing a trade barrier in fresh horticultural products. In Kenya, Liriomyza species attack a variety of horticultural commercial value crops including snow pea (Pisum sativum (L.; Fabales: Fabaceae)), French bean (Phaseolus vulgaris (L.; Fabales: Fabaceae)), runner bean (Phaseolus coccineus (L.; Fabales: Fabaceae)), tomato (Lycospersicon esculentum (Miller; Solanales: Solanaceae)), potato (Solanum tuberosum (L.; Solanales: Solanaceae)), Eryngium sp. (L.; Apiales: Apiaceae), Gypsophila sp. (L.; Caryophyllales: Caryophyllaceae), and Carthamus sp. (L.; Asterales: Asteraceae) cut flowers (Chabi-Olaye et al. 2008, KEPHIS 2014, Foba et al. 2015b, Guantai et al. 2015). Horticulture is an important sector of agriculture providing employment to millions of people and generating foreign currency (McCulloch and Ota 2002, NHP 2012, KHC 2015). It contributes on average 25.3% of Kenya’s Gross Domestic Product (GDP and earned the country $2 billion in 2013 (KNBS 2015, KFC 2014). Several pesticide including organophosphates, carbamates, pyrethroids, and triazines (cryomazine) have been identified and adversely used for Liriomyza leafminer control which if used exclusively could quickly generate resistance (Weintraub and Horowitz 1997, Price and Nagle 2002, Guantai et al. 2015). The indiscriminate use of insecticides is likely to be one of the reasons for the leafminer outbreaks in their invaded ranges with negative effects to their natural enemies (Murphy and LaSalle 1999, Gitonga et al. 2010). In recent years, pesticide residues above acceptable levels have become a technical trade to barrier in horticultural products in the European market (RASFF 2014). In their native ranges, natural enemies are important in regulating Liriomyza species populations (Shepard et al. 1998, Murphy and LaSalle 1999, Rauf et al. 2000, Mujica and Kroschel 2011). More than 300 species of parasitoids are associated with leafminers worldwide (Noyes 2003). In Peru, a complex of 63 parasitoid species is associated with Liriomyza leafminers causing high leafminer mortality of between 20 and 55% (Mujica and Kroschel 2011). In contrast, the diversity of existing Liriomyza parasitoids in East Africa field crops is low with parasitism rates below 6% (Chabi-Olaye et al. 2008). Parasitoids associated with Liriomyza leafminers mainly comprises of Diglyphus isaea (Walker), Neochrysocharis formosa (Westwood; Hymenoptera: Eulophidae)), Hemiptarsenus varicornis (Girault; Hymenoptera: Eulophidae), and Opius dissitus (Muesebeck; Hymenoptera: Braconidae), (Chabi-Olaye et al. 2008, Guantai et al. 2015, Foba et al. 2015c). In view of improving biological control of Liriomyza leafminers and further boosting the parasitism rates in East Africa, Halticoptera arduine (Walker; Hymenoptera: Pteromalidae) was imported from Peru into Kenya by the International Centre of Insect Physiology and Ecology (ICIPE), Nairobi, in collaboration with the International Potato Centre (CIP), under Leafminer IPM program. H. arduine is a larval endoparasitoid of Agromyzid leafminers which completes its development within the host. After parasitization, the host larva continues to develop into pupal stage until the adult parasitoid emerges from the host pupal case. Shortly after emergence, adult female parasitoids begin searching for leafminer larvae on leaf surfaces and on encounter, deposits up to three eggs in one host but only one offspring develops per host (Arellano and Redolfi 1989). Sex ratio of H. arduine is affected by host density and fertilization of females where unfertilized females produce only males (Kroschel et al. 2016). Low (<10°C) and high (>30°C) temperatures also affect the reproduction and development of H. arduine (Prudencio 2010). However, not much on H. arduine biology including its searching behavior, host specificity studies, or its use in classical biological control programs has been reported. In its native origins, H. arduine is adapted to a wide range of ecological areas efficiently parasitizing up to seven species of Agromyzid leafminer fly species in a range of 25 host plants causing up to 67% parasitism rates (Sanchez and Redolfi 1989, Neder de Romȃn 2000, Mujica and Kroschel 2011, Kroschel et al. 2016). The potential performance of the exotic parasitoid in controlling local Liriomyza species needed an evaluation before its consideration for a classical biological control program. This acceptability research will address the questions as to whether H. arduine will search and accept to oviposit in three local Liriomyza host species. The suitability studies will provide answers to the question on whether eggs will complete development within the hosts, parasitoid performance, and their fitness in these three host species. The objective of this study was therefore to evaluate the acceptability and suitability of H. arduine to three Liriomyza species found in Kenya before its consideration for introduction as a biological control agent. MATERIALS AND METHODS Plant Materials Fourteen-days-old potted plants of faba bean, Vicia faba (L.; Fabales: Fabaceae) and rose coco beans, P. vulgaris L. (Fabales: Fabaceae) were raised and supplied from screen house at the International Center of Insect Physiology and Ecology (ICIPE) Duduville campus in Kenya in conical plastic pots (5.5 cm diameter and 7.3 cm height) with five plants per pot. Insect Colonies Leafminer colonies Colonies of L. huidobrensis were initiated from field collections in Nyeri (0°21′S, 36°57′E, 2200 m.a.s.l) in Central Kenya highlands of Nyeri County and reared on V. faba. V. faba was chosen because it had been found as the best host plant for laboratory rearing and maintenance of L. huidobrensis (Videla et al. 2006, Chabi-Olaye et al. 2013). L. sativae and L. trifolii colonies were initiated from field collections in Kibwezi (02°15′S 37°49′E, 965 m.a.s.l), Makindu (02°16′S 37°48′E, 991 m.a.s.l) and Masongaleni (02°22′S 38°08′E, 714 m.a.s.l) in the Eastern low-lying counties of Kenya (Chabi-Olaye et al. 2013) and reared on rose coco beans. Musundire et al. (2012) and Okoth (2011) reported that L. sativae and L. trifolii preferred P. vulgaris compared to other tested host plants for oviposition and development and this led to the use of P. vulgaris as experimental host plant. The colonies were reared in Perspex cages (60 cm length × 60 width × 60 cm) (made at icipe, Nairobi, Kenya) under species-specific controlled temperatures and humidity that were optimum for their development (Okoth 2011, Musundire et al. 2012, Foba et al. 2015b) (25 ± 2°C and 55 ± 5% RH for L. huidobrensis and 27 ± 2°C and 55 ± 5% RH for L. sativae and L. trifolii). Adult leafminers were fed on 10% sugar solution for 2 d after emergence before exposure to host plants for experimental use. Halticoptera arduine colony Initial culture of H. arduine, a solitary endoparasitoid of Liriomyza leafminers, was obtained from the International Potato Center (CIP) in Peru, where they were maintained on L. huidobrensis. The parasitoid was maintained in the quarantine facility at ICIPE on L. huidobrensis at 25°C ± 1 and 55–60% RH for 12 generations after establishment before its experimental use. Newly emerged parasitoids were maintained on honey solution as source of food for 2 d before their exposure to the host insect larvae. Experimental procedure The first set of acceptability experiments were conducted separately from the second set of suitability experiments which were sequentially conducted after the acceptability experiments. The acceptability experiment study was conducted using methodology described by Chabi-Olaye et al. (2013) in the assessment of Phaedrotoma scabriventris (Nixon; Hymenoptera: Braconidae) acceptability to three Liriomyza species. Procedures described by Chabi-Olaye et al. (2013) were used for suitability studies with slight modifications. Chabi-Olaye et al. (2013) used excised plants with only two infested leaves and immersed in water in 10-ml glass vial and 10 female parasitoids per replicate. In the present study, however, 50 infested whole-potted plants (10 pots × 5 plants/pot) were held per Perspex cage and 50 2-d-old H. arduine adults (1 male: 2 females) were released per replicate. In host acceptance experiments, faba bean plants were exposed to 2-d-old adults of L. huidobrensis for 24 h for egg laying and maintained in a cage for 5 to 6 d to get a cohort of same age larvae. A two-leaved faba bean stem infested by between 10- and 15-s third larval stages of L. huidobrensis was excised above the soil base and inserted into a glass vial (30 ml) in upright position supported by moist cotton wool. The set up was placed in clear Perspex cage (15 × 15 × 20 cm) with the top and sides covered by fine insect netting (150 × 150 µm) for aeration in controlled environment (25°C ± 1 and 55–60% RH) using a thermostatic electric heater (Xpelair, United Kingdom) and humidifier. A 2-d-old naive mated female adult of H. arduine was introduced into the cage. The behavioral activities of the parasitoid on the infested plant (time spent on host searching and encounter and number of oviposition attempts) were directly recorded by visual observation for a 2-h period per replicate. After the 2-h period, the female parasitoid was removed and the larvae incubated (25°C ± 1 and 55–60% RH) in plastic Petri dish for 3 d to allow for pupae development. After 6 d, each individual pupa was incubated (25°C ± 1 and 55–60% RH) in gelatin capsule (2.20 cm height and 0.7 cm diameter) for 8 to 16 d until adult leafminer or parasitoid emergence. Under these experimental conditions, average developmental times were 14 and 25 d for leafminer and parasitoid, respectively. The number of female parasitoids with successful oviposition in each host was confirmed by emergence or recovery of a parasitoid. The experiment was replicated 40 times and the same experimental set up was repeated using L. sativae and L. trifolii on P. vulgaris. In our second experiment, 200 2-d-old L. huidobrensis (at the ratio of 1 male: 2 females) were exposed to 10 pots of 2-wk-old faba bean plants (five plants/pot) for 24-h in Perspex cages (30 × 30 × 45 cm) with two sides covered by fine insect netting (150 × 150 µm) for aeration. The exposure of L. huidobrensis was done in 10 cages, five of which received the parasitoid treatment and five represented control with no parasitoids. Infested plants were held for 5 to 6 d to allow the development of same age cohort of second–third larval stages of leafminer. A batch of 50 2-d-old adult H. arduine parasitoids (at the ratio of 1 male: 2 females) were released in the five Perspex cages containing the infested plants for 24-h before removal. The host larvae were held on the plants for 5 to 6 d for pupae development. Each pupa was capsulated and incubated (25°C ± 1 and 55–60% RH) in transparent gelatin capsules (2.20 cm height and 0.7 cm diameter) for adult leafminers and parasitoids emergence. The control allowed for assessment of leafminer natural mortality. The same methodology was repeated for L. sativae and L. trifolii hosts reared on P. vulgaris at different times. This experiment thus, consisted of three treatments and each of the treatment represented a Liriomyza host species replicated five times alongside with a control in a completely randomized design. In both experiments, the number of pupae, emerged leafminer adults and first generation parasitoids (F1 offspring), F1 parasitoids developmental period, and sex ratio were recorded. Pupae without exit holes and with unemerged insects were dissected under Leica EZ4D binocular microscope (Leica Microsystems Switzerland Ltd 2007; Glattbrugg, Switzerland; LAS EZ V 1.5.0 software (LEITZ, Glattbrugg, Switzerland)) following the methodology described by Heinz and Parrella (1990) to correct parasitism rate and nonreproductive host mortality. Nonreproductive host mortality was expressed as a percentage of unviable pupae over the total pupae in each treatment as described by Foba et al. (2015a). The right forewing and right hind tibia of 10 randomly selected male and female F1 parasitoids were detached from the point of contact with thorax and images taken using Leica EZ4D microscope camera (Leica Microsystems Switzerland Ltd 2007; LAS EZ V 1.5.0 software (LEITZ)). Wings and hind tibia were spread in 70% ethanol and the lengths measured at 35× magnification (Heinz and Parrella 1990, Honek 1993, Videla et al. 2006, Okoth et al. 2014). Data Analyses For each Liriomyza species, absolute numbers of F1 progeny males and females parasitoids and dead pupae were analyzed using Chi-square test in R version 3.0.2 statistical software (R Development Core Team 2013) to determine differences in sex ratio and significance level of nonreproductive mortalities. Count data on searching time, oviposition attempts, developmental time, and number of parasitoids in a progeny and percentage data on parasitism rates, sex ratios, and mortalities were log and arcsine transformed, respectively, before being subjected to one-way analysis of variance. Where there was significant difference between Liriomyza species in regards to time taken for a female parasitoid to first encounter host, oviposition attempts made on larval hosts in a 2-h observation period, proportion of female parasitoids that successfully oviposited in the hosts, number of parasitoids in F1 progeny from each host, developmental time of F1 parasitoids, parasitism rates, pupal mortality, and body size indices, means were separated using Tukey–Kramer honest significant difference test (P < 0.05) (SAS 2013, JMP V11, 2013). Results Host Acceptance Results of H. arduine acceptability to Liriomyza host species after 2 h are presented in Table 1. The parasitoid accepted and successfully deposited eggs in the three Liriomyza species, with up to 97.50 ± 2.50 (means ± SE) % of females laying eggs in L. sativae and L. trifolii. The number of oviposition attempts per female within 2-h observation period were also high, ranging from 57.30 ± 2.06 to 66.20 ± 3.48, with a significantly higher number of oviposition attempts on L. huidobrensis compared to L. sativae and L. trifolii (F2,117 = 4.07, P = 0.0196). Females parasitoids took a short period of time (as low as 10.45 ± 0.83 to 13.30 ± 1.37 s) to search and encounter their first host for oviposition with significantly shorter time (F2,117 = 7.98, P = 0.0006) spent on L. trifolii than on L. sativae. However, searching and encountering time on L. huidobrensis was not significantly different from that observed on L. sativae and L. trifolii. Significantly more females parasitoids successfully oviposited in L. sativae and L. trifolii than in L. huidobrensis (F2,117 = 14.91, P < 0.0001) (Table 1). Table 1. Acceptability parameters of three Liriomyza species to Halticoptera arduine (mean ± SE) under laboratory conditions (25°C ± 1 and 55–60% RH) Variable indicator Liriomyza huidobrensis Liriomyza sativae Liriomyza trifolii Time taken (s) to search and encounter first host 13.30 ± 1.37ab 15.80 ± 0.91a 10.45 ± 0.83b Mean number of oviposition attempts per female parasitoid 66.20 ± 3.48a 57.38 ± 1.73b 57.30 ± 2.06b Proportion of female parasitoids with successful oviposition (%) 65.00 ± 7.64b 97.50 ± 2.50a 97.50 ± 2.50a Variable indicator Liriomyza huidobrensis Liriomyza sativae Liriomyza trifolii Time taken (s) to search and encounter first host 13.30 ± 1.37ab 15.80 ± 0.91a 10.45 ± 0.83b Mean number of oviposition attempts per female parasitoid 66.20 ± 3.48a 57.38 ± 1.73b 57.30 ± 2.06b Proportion of female parasitoids with successful oviposition (%) 65.00 ± 7.64b 97.50 ± 2.50a 97.50 ± 2.50a (s)- second, within row, means followed by the same letter are not significantly different at P ≤ 0.05 (Tukey–Kramer test). View Large Table 1. Acceptability parameters of three Liriomyza species to Halticoptera arduine (mean ± SE) under laboratory conditions (25°C ± 1 and 55–60% RH) Variable indicator Liriomyza huidobrensis Liriomyza sativae Liriomyza trifolii Time taken (s) to search and encounter first host 13.30 ± 1.37ab 15.80 ± 0.91a 10.45 ± 0.83b Mean number of oviposition attempts per female parasitoid 66.20 ± 3.48a 57.38 ± 1.73b 57.30 ± 2.06b Proportion of female parasitoids with successful oviposition (%) 65.00 ± 7.64b 97.50 ± 2.50a 97.50 ± 2.50a Variable indicator Liriomyza huidobrensis Liriomyza sativae Liriomyza trifolii Time taken (s) to search and encounter first host 13.30 ± 1.37ab 15.80 ± 0.91a 10.45 ± 0.83b Mean number of oviposition attempts per female parasitoid 66.20 ± 3.48a 57.38 ± 1.73b 57.30 ± 2.06b Proportion of female parasitoids with successful oviposition (%) 65.00 ± 7.64b 97.50 ± 2.50a 97.50 ± 2.50a (s)- second, within row, means followed by the same letter are not significantly different at P ≤ 0.05 (Tukey–Kramer test). View Large Host Suitability The three Liriomyza hosts tested were found suitable for H. arduine. The parasitoid took between 19.32 ± 0.96 and 22.86 ± 0.27 d to complete development from egg to adult in the three hosts. H. arduine parasitized significantly more L. huidobrensis than L. sativae (F2,12 = 4.05, P = 0.0452); however, the parasitism in L. trifolii was similar to the two other hosts (Table 2). Liriomyza hosts affected sex ratio of H. arduine F1 progeny with a significant female-biased sex ratio when reared on L. huidobrensis (χ2 = 18.84, P < 0.0001) compared to a balanced sex ratio when reared on L. sativae (χ2 = 0.00, P = 1.00) and a male biased when reared on L. trifolii (χ2 = 18.84, P < 0.0001). Across the treatments, the proportion of female parasitoids’ in F1 were not significantly different (F2,79 = 4.67, P = 0.4798) (Table 2). Table 2. Host suitability—effect of Liriomyza host species on Halticoptera arduine developmental time, parasitism rate, and sex ratio (mean ± SE) under laboratory conditions (25°C ± 1 and 55–60% RH) Variable indicator Liriomyza huidobrensis Liriomyza sativae Liriomyza trifolii F1 developmental time (d) 19.32 ± 0.96c 21.23 ± 0.16b 22.86 ± 0.27a Parasitism rate (%) 44.10 ± 4.56a 27.96 ± 3.86b 32.28 ± 3.65ab Proportion of female parasitoids in F1 progeny (%) 57.94 ± 9.32aA 49.32 ± 5.59aA 45.31 ± 6.43aB Proportion of male parasitoids in F1 progeny (%) 42.03 ± 9.32aB 50.68 ± 5.59aA 54.69 ± 6.43aA Mean number of parasitoids in F1 progeny 33.0 ± 5.11b 61.80 ± 2.15a 61.00 ± 4.83a Variable indicator Liriomyza huidobrensis Liriomyza sativae Liriomyza trifolii F1 developmental time (d) 19.32 ± 0.96c 21.23 ± 0.16b 22.86 ± 0.27a Parasitism rate (%) 44.10 ± 4.56a 27.96 ± 3.86b 32.28 ± 3.65ab Proportion of female parasitoids in F1 progeny (%) 57.94 ± 9.32aA 49.32 ± 5.59aA 45.31 ± 6.43aB Proportion of male parasitoids in F1 progeny (%) 42.03 ± 9.32aB 50.68 ± 5.59aA 54.69 ± 6.43aA Mean number of parasitoids in F1 progeny 33.0 ± 5.11b 61.80 ± 2.15a 61.00 ± 4.83a (d)-days, within row and for the same variable, means followed by the same lower case letter are not significantly different at P ≤ 0.05 (Tukey–Kramer test). For each Liriomyza species, means followed by same upper case letter for male and female are not significantly different at P ≤ 0.05 (Chi-square test). View Large Table 2. Host suitability—effect of Liriomyza host species on Halticoptera arduine developmental time, parasitism rate, and sex ratio (mean ± SE) under laboratory conditions (25°C ± 1 and 55–60% RH) Variable indicator Liriomyza huidobrensis Liriomyza sativae Liriomyza trifolii F1 developmental time (d) 19.32 ± 0.96c 21.23 ± 0.16b 22.86 ± 0.27a Parasitism rate (%) 44.10 ± 4.56a 27.96 ± 3.86b 32.28 ± 3.65ab Proportion of female parasitoids in F1 progeny (%) 57.94 ± 9.32aA 49.32 ± 5.59aA 45.31 ± 6.43aB Proportion of male parasitoids in F1 progeny (%) 42.03 ± 9.32aB 50.68 ± 5.59aA 54.69 ± 6.43aA Mean number of parasitoids in F1 progeny 33.0 ± 5.11b 61.80 ± 2.15a 61.00 ± 4.83a Variable indicator Liriomyza huidobrensis Liriomyza sativae Liriomyza trifolii F1 developmental time (d) 19.32 ± 0.96c 21.23 ± 0.16b 22.86 ± 0.27a Parasitism rate (%) 44.10 ± 4.56a 27.96 ± 3.86b 32.28 ± 3.65ab Proportion of female parasitoids in F1 progeny (%) 57.94 ± 9.32aA 49.32 ± 5.59aA 45.31 ± 6.43aB Proportion of male parasitoids in F1 progeny (%) 42.03 ± 9.32aB 50.68 ± 5.59aA 54.69 ± 6.43aA Mean number of parasitoids in F1 progeny 33.0 ± 5.11b 61.80 ± 2.15a 61.00 ± 4.83a (d)-days, within row and for the same variable, means followed by the same lower case letter are not significantly different at P ≤ 0.05 (Tukey–Kramer test). For each Liriomyza species, means followed by same upper case letter for male and female are not significantly different at P ≤ 0.05 (Chi-square test). View Large In the three Liriomyza hosts studied, H. arduine did not induce any significantly different nonreproductive host mortality in three hosts from the control (PLh = 0.0639, PLs = 0.2345, and PLt = 0.6155) (Table 3). Table 3. Host suitability—nonreproductive host mortality by Halticoptera arduine in three Liriomyza host species (means ± SE) under laboratory conditions (25°C ± 1 and 55–60% RH) Liriomyza huidobrensis Liriomyza sativae Liriomyza trifolii Host mortality in presence of parasitoids (%) 50.55 ± 4.58Aa 37.32 ± 2.97Aa 40.81 ± 2.36Aa Natural host mortality in control (%) 33.32 ± 2.99Aa 41.77 ± 2.17Aa 39.40 ± 1.98Aa χ2 3.43 1.41 0.25 P value 0.0639 0.2345 0.6155 Liriomyza huidobrensis Liriomyza sativae Liriomyza trifolii Host mortality in presence of parasitoids (%) 50.55 ± 4.58Aa 37.32 ± 2.97Aa 40.81 ± 2.36Aa Natural host mortality in control (%) 33.32 ± 2.99Aa 41.77 ± 2.17Aa 39.40 ± 1.98Aa χ2 3.43 1.41 0.25 P value 0.0639 0.2345 0.6155 Within rows (columns), means followed by the same lower (upper) case letter are not significantly different at P ≤ 0.05 (Tukey–Kramer) and (Chi-square) test in that respect. View Large Table 3. Host suitability—nonreproductive host mortality by Halticoptera arduine in three Liriomyza host species (means ± SE) under laboratory conditions (25°C ± 1 and 55–60% RH) Liriomyza huidobrensis Liriomyza sativae Liriomyza trifolii Host mortality in presence of parasitoids (%) 50.55 ± 4.58Aa 37.32 ± 2.97Aa 40.81 ± 2.36Aa Natural host mortality in control (%) 33.32 ± 2.99Aa 41.77 ± 2.17Aa 39.40 ± 1.98Aa χ2 3.43 1.41 0.25 P value 0.0639 0.2345 0.6155 Liriomyza huidobrensis Liriomyza sativae Liriomyza trifolii Host mortality in presence of parasitoids (%) 50.55 ± 4.58Aa 37.32 ± 2.97Aa 40.81 ± 2.36Aa Natural host mortality in control (%) 33.32 ± 2.99Aa 41.77 ± 2.17Aa 39.40 ± 1.98Aa χ2 3.43 1.41 0.25 P value 0.0639 0.2345 0.6155 Within rows (columns), means followed by the same lower (upper) case letter are not significantly different at P ≤ 0.05 (Tukey–Kramer) and (Chi-square) test in that respect. View Large Parasitoid fitness on the various Liriomyza hosts in F1 offspring are presented in Table 4. The forewing of H. arduine measured between 1.27 ± 0.04 and 1.43 ± 0.10 mm for the females and 1.19 ± 0.03 to 1.34 ± 0.02 mm for the males. The hind tibia length of the female parasitoids measured between 0.35 ± 0.01 and 0.40 ± 0.01 while that in the males measured between 0.34 ± 0.01 and 0.41 ± 0.02. Female parasitoids reared on L. huidobrensis had significantly longer forewing than those reared on L. trifolii while those of L. sativae did not significantly differ from either of the two hosts (F2,27 = 4.59, P = 0.0192). Similarly, female parasitoids reared on L. huidobrensis had significantly longer hind tibia than those reared on L. sativae and L. trifolii (F2,27 = 5.37, P = 0.0109) (Table 4). On the other hand, male parasitoids reared on L. trifolii and L. huidobrensis, had significantly longer forewing than those reared on L. sativae (F2,27 = 7.94, P = 0.0019) while their hind tibia were significantly longer for those reared on L. trifolii than from L. sativae. Hind tibia from L. huidobrensis were not significantly different from the two former hosts (F2,27 = 7.14, P = 0.0032). There was no significance difference in parasitoid wing and tibia lengths between male and females within host (L. huidobrensis: χ2 = 0.01, P = 0.9137 and χ2 = 0, P = 1; L. sativae: χ2 = 0.05, P = 0.8316 and χ2 = 0, P = 1; L. trifolii: χ2 = 0.0.01, P = 0.9294 and χ2 = 0, P = 1, respectively) (Table 4). Table 4. Host suitability—effect of Liriomyza host species on adult Halticoptera arduine fitness (means ± SE) under laboratory conditions (25°C ± 1 and 55–60% RH) Parasitoid body size indices Liriomyza huidobrensis Liriomyza sativae Liriomyza trifolii Forewing length (mm)  Females 1.43 ± 0.03aA 1.37 ± 0.04abA 1.27 ± 0.04bA  Males 1.29 ± 0.03aA 1.19 ± 0.03bA 1.34 ± 0.02aA  χ2 0.0118 0.0452 0.0079  P value 0.9137 0.8316 0.9294 Hind tibia length (mm)  Females 0.40 ± 0.01aA 0.36 ± 0.01bA 0.35 ± 0.01bA  Males 0.37 ± 0.01abA 0.34 ± 0.01bA 0.41 ± 0.02aA  χ2 0 0 0  P value 1 1 1 Parasitoid body size indices Liriomyza huidobrensis Liriomyza sativae Liriomyza trifolii Forewing length (mm)  Females 1.43 ± 0.03aA 1.37 ± 0.04abA 1.27 ± 0.04bA  Males 1.29 ± 0.03aA 1.19 ± 0.03bA 1.34 ± 0.02aA  χ2 0.0118 0.0452 0.0079  P value 0.9137 0.8316 0.9294 Hind tibia length (mm)  Females 0.40 ± 0.01aA 0.36 ± 0.01bA 0.35 ± 0.01bA  Males 0.37 ± 0.01abA 0.34 ± 0.01bA 0.41 ± 0.02aA  χ2 0 0 0  P value 1 1 1 Within rows (columns and for each parameter), means followed by the same lower (upper) case letter are not significantly different at P ≤ 0.05 according to Tukey–Kramer (Chi-square) test. View Large Table 4. Host suitability—effect of Liriomyza host species on adult Halticoptera arduine fitness (means ± SE) under laboratory conditions (25°C ± 1 and 55–60% RH) Parasitoid body size indices Liriomyza huidobrensis Liriomyza sativae Liriomyza trifolii Forewing length (mm)  Females 1.43 ± 0.03aA 1.37 ± 0.04abA 1.27 ± 0.04bA  Males 1.29 ± 0.03aA 1.19 ± 0.03bA 1.34 ± 0.02aA  χ2 0.0118 0.0452 0.0079  P value 0.9137 0.8316 0.9294 Hind tibia length (mm)  Females 0.40 ± 0.01aA 0.36 ± 0.01bA 0.35 ± 0.01bA  Males 0.37 ± 0.01abA 0.34 ± 0.01bA 0.41 ± 0.02aA  χ2 0 0 0  P value 1 1 1 Parasitoid body size indices Liriomyza huidobrensis Liriomyza sativae Liriomyza trifolii Forewing length (mm)  Females 1.43 ± 0.03aA 1.37 ± 0.04abA 1.27 ± 0.04bA  Males 1.29 ± 0.03aA 1.19 ± 0.03bA 1.34 ± 0.02aA  χ2 0.0118 0.0452 0.0079  P value 0.9137 0.8316 0.9294 Hind tibia length (mm)  Females 0.40 ± 0.01aA 0.36 ± 0.01bA 0.35 ± 0.01bA  Males 0.37 ± 0.01abA 0.34 ± 0.01bA 0.41 ± 0.02aA  χ2 0 0 0  P value 1 1 1 Within rows (columns and for each parameter), means followed by the same lower (upper) case letter are not significantly different at P ≤ 0.05 according to Tukey–Kramer (Chi-square) test. View Large Discussion Parasitoids spend a significant amount of time searching for hosts, while a significant amount of time is spent probing the host to assess their suitability before making the decision to oviposit. The success of parasitoid–host relationship assumes a hierarchy of discrete steps that include habitat location, host location, host acceptance, host suitability (Doutt 1959, Vinson 1976), and host regulation (Vinson and Iwantsch 1980). Vinson (1975) considered host acceptance as the most important step for parasitoid success. H. arduine, the exotic endoparasitoid of Liriomyza leafminer accepted to oviposit and developed successfully in the three common Liriomyza hosts found in Kenya. Previous studies on the searching behavior of H. arduine showed that females encountered L. huidobrensis larvae immediately on their introduction to V. faba infested plants (Prudencio 2010). This concurs with our observations on the three Liriomyza hosts. Plant physical and chemical characteristics have an effect on searching time, movement, and foraging success of parasitoids (Andow and Prokrym 1990, Lukianchuk and Smith 1997, Lovinger et al. 2000, Suverkropp et al. 2001, Wang and Keller 2002). However, H. arduine searching behavior seemed not to be affected by host plant. Searching time on L. huidobrensis reared on V. faba was not different from the one on L. sativae and L. trifolii, both reared on P. vulgaris. The significant difference was rather between L. sativae and L. trifolii despite both being reared on the same plant. We, therefore, hypothesize that pest–host interaction could have influenced the searching behavior of H. arduine and thus recommend further studies to elucidate potential difference in chemical profile resulting from infestation of P. vulgaris by L. trifolii. Oviposition attempt by female parasitoids is considered as an important behavioral measurement for parasitoid host acceptance (Agboka et al. 2002). Considering the number of oviposition attempts made by H. arduine female on each of the Liriomyza hosts as selection decision for oviposition, it is evident that L. huidobrensis was a better choice for oviposition than L. sativae and L. trifolii, which also translated to a high parasitism rate on this host. Among the factors which influence the success of parasitoid development is the stage or instar at parasitization (Hegazi and Khafagi 2005). H. arduine prefers late second and early third larval instars of Liriomyza hosts for oviposition and parasitization (Arellano and Redolfi 1989) during which development to adult takes place. Results from this study showed that H. arduine completed its development within the three Liriomyza host species and our results were similar to that reported by Prudencio (2010) when reared on L. huidobrensis. This implies that H. arduine will successfully develop in the existing Liriomyza species occurring in Kenya’s agro-ecological systems and contribute to their natural control. However, further studies are required to assess its potential competition, complementarities or coexistence with indigenous parasitoids already present in the system. Various indigenous and exotic leafminer parasitoids have been reported in Kenya and this include mainly D. isaea, O. dissitus, and P. scabriventris which represent 95.18% of total parasitoids recorded at low, mid, and high altitudes of Kenya (Foba et al. 2015c). Male parasitoids only mate and do not contribute to pest mortality (Hassel et al. 1983, Comins and Wellings 1985). Male-biased populations of H. arduine have been reported by Arellano and Redolfi (1989), Neder de Romȃn (2000), and Prudencio (2010) when H. arduine was reared on low host population of L. huidobrensis and from lower and higher temperature developmental thresholds. The reverse was true when H. arduine was reared in high population of L. huidobrensis. (Neder de Romȃn, 2000). In contrast to these findings, our study revealed a female-biased and balanced sex ratio in L. huidobrensis and L. sativae hosts, respectively. In parasitoids, a balanced or female-biased sex ratio infers stability and higher efficiency compared to a male-biased one, as only females directly contribute to the mortality of pests (Beddington et al. 1978, Mills and Getz 1996, Ode and Heinz 2002, Pascua and Pascua 2004, Chow and Heinz 2005, Abe and Kamimura 2012, Foba et al. 2015a). Our results, therefore, suggest better reproduction potential for H. arduine in regards to the local populations of L. huidobrensis, L. sativae, and L. trifolii in Kenya. With insects, there is generally a positive relationship between body size and performance (Clutton-Brock 1988, Honek 1993) and fitness (Stoepler et al. 2011). The success of parasitoid to develop and complete its life cycle in a suitable host is influenced by other factors, host size (Lawrence 1990) which positively correlates with adult parasitoid size (Spencer 1990, Visser 1994, Lampson et al. 1996, Fidgen et al. 2000, Roitberg et al. 2001, Teder and Tammaru 2002). Additionally, performance of Agromyzid leafminer parasitoids depends on the body size of their hosts (Heinz and Parrella 1990, Spencer 1990, Salvo and Valladares, 1995, Ode and Heinz, 2002). However, host size is not necessarily the only indicator of parasitoid performance and other factors such as host plants can influence parasitoid performance (Salvo and Valladares 2002, Tran et al. 2007, Musundire et al. 2010). In our present studies, H. arduine female progeny reared on L. huidobrensis were larger than those reared on L. sativae and L. trifolii. In similar studies, Neochrysocahris okazakii (Kamijo; Hymenoptera: Eulophidae) reared on Liriomyza chinensis (Kato; Diptera: Agromyzidae) were larger than those reared on L. trifolii (Tran and Takagi 2005, Tran et al. 2007). Similarly P. scabriventris reared on L. huidobrensis were found to be larger than those reared on L. sativae and L. trifolii (Chabi-Olaye et al. 2013). It is assumed that larger hosts represent greater resource quantity for parasitoid development (Charnov 1982, Charnov and Skinner 1985) and performance (fecundity) (Musundire et al. 2012) with greater longevity, better searching capacity, and higher dispersal ability (Godfray 1994, Visser 1994). Studies by Spencer (1973) and Musundire et al. (2012) have confirmed that L. huidobrensis is larger in body size than L. sativae and L. trifolii. This suggests that the body size of the host affected the fitness of the parasitoid in the present study. Nonreproductive host mortality caused by parasitoids has been reported to constitute an important component in pest suppression in many studies (Sandlan 1979, Walter 1988, Tran and Takagi 2006, Bernardo et al. 2006, Akutse et al. 2015). However, this is more commonly reported among ectoparasitoids than in endoparasitoids. For example, Mafi and Ohbayashi (2010) observed that Sympiesis striatipes (Ashmead; Hymenoptera: Eulophidae) an ectoparasitoid, caused nonreproductive mortality of 44.7 ± 4.2% on citrus leafminer, Phyllocnistis citrella (Stainton; Lepidoptera: Gracillariidae). Similarly, female wasps of D. isaea were reported to cause significant nonreproductive mortality of Liriomyza larvae by host feeding and stinging without oviposition (Minkenberg 1989, Liu et al. 2013, Akutse et al. 2015). Copidosoma koehleri (Blanchard; Hymenoptera: Encyrtidae), an egg-larval endoparasitoid of potato tuber moth Phthorimaea operculella (Zeller; Lepidoptera: Gelechiidae) is one of the few exceptions of endoparasitoids reported to cause nonreproductive mortality (Keinan et al. 2012). In the present study, no significant nonreproductive host mortalities were recorded in H. arduine in any of the three host’s studies. These results concur with the findings of Prudencio (2010) who reported nonreproductive mortalities as low as 7% in H. arduine when reared on L. huidobrensis. Similar findings of such poor endoparasitoid-induced nonreproductive host mortality in Liriomyza leafminer were reported by Chabi-Olaye et al. (2013) and Foba et al. (2015a) while studying the performance of P. scabriventris against L. huidobrensis. In conclusion, this study has established that H. arduine can accept to oviposit and develop successfully in the three most economically important Liriomyza leafminers in East Africa and was not affected by host plant. The performance of the parasitoid should also be mainly based on its parasitism potential since it caused no significant nonreproductive mortality in the hosts. Parasitism rates, fitness, and sex-ratio parameters of the parasitoid were all promising. Considering that the three Liriomyza leafminer species studied are the most important across Africa, we hypothesize that H. arduine can successfully establish and contribute to the control of Liriomyza leafminers in Africa in general and particularly in Kenya. Pilot sites and open-field release activities are warranted to test and confirm this hypothesis. However, prior to this, to ensure that local parasitoid populations are not displaced by the exotic species, interaction studies between H. arduine and the parasitoids already existing in the system are warranted. Acknowledgments The authors are grateful to Jürgen Kroschel and Norman Mujica of the International Potato Center (CIP) in Peru for providing H. arduine specimens to start the colony in Kenya. The first author was supported through the Dissertation and Research Internship Program (DRIP) of icipe. The present study was conducted with financial support from the German Federal Ministry for Economic Cooperation and Development (BMZ) (Grant number: 09.7860.1-001.00; Contract number: 81121261). We are also grateful to UK Aid of the UK Government, the Swedish International Development Cooperation Agency (Sida), the Swiss Agency for Development and Cooperation (SDC), and the Kenyan Government for their core support to icipe that facilitated the present work. 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Published: Apr 13, 2018

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