Journal of Asia-Pacific Entomology 21 (2018) 676–681

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Journal of Asia-Pacific Entomology

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Full Length Article Starving asychis negatively affects host feeding and parasitism on T Myzus persicae

Sheng-Yin Wanga,b, Yi Fengb, Ning-Ning Liangb, Rui Tangb, Yan-Hong Liub, Da Yu Zhanga, ⁎ Tong-Xian Liub, a College of Agriculture and Food Science, Zhejiang A&F University, Hangzhou 311300, Zhejiang, China b State Key Laboratory of Crop Stress Biology for Arid Areas, Key Laboratory of Northwest Loess Plateau Crop Pest Management of Ministry of Agriculture, Northwest A&F University, Yangling 712100, Shaanxi, China

ARTICLE INFO ABSTRACT

Keywords: Aphelinus asychis (Walker) is an effective biological control agent for many species of aphids found on various Aphelinus asychis crops. To provide strategies for releasing these parasitoids into a crop ecosystem, the effects of a short-duration Myzus persicae starvation experiment on A. asychis were measured under laboratory conditions using Myzus persicae (Sulzer) as Duration of starvation the host on cabbage and chili pepper plants. The survival rate of starved A. asychis female adults decreased Chili pepper sharply as the starving time increased, and the longevity of the starved parasitoids also decreased significantly. Cabbage The number of aphids killed by the parasitoids decreased gradually with the extended duration of starvation. In addition, the number of aphids on chili peppers and cabbages killed by starved A. asychis females over their lifespan was significantly lower than that in the control group. Our results indicated that a short period of starvation might not cause significantly negative effects on the parasitoids and may be beneficial for the control of M. persicae at low densities after 1 day; however, starvation for > 1 day seriously affected the performance of A. asychis females over their entire lifespan. The parasitoids performed similarly when aphids were fed chili pepper or cabbage plants.

Introduction The majority of species belonging to the genus Aphelinus Dalman are parasitoids of aphids (Hemiptera: Aphidoidea) and are important for The green peach aphid, Myzus persicae (Sulzer) (Hemiptera: controlling aphid pests (Hayat, 1983). A. asychis (Walker) (Hyme- Aphididae), is an extremely cosmopolitan agricultural pest species that noptera: ) is an arrhenotokous parthenogenetic en- is found worldwide (van Emden and Harrington, 2007). There are many doparasitoid of aphids, probably native to the Old World (Zhu and factors that enhance the status of this species as a pest, including host Fang, 2009), and can parasitize up to 40 aphid species, including Si- range, damage mechanisms to plants, and life cycle (Bass et al., 2014). tobion avenae (Fabricius) (Homoptera: Aphididae) (Wang et al., 2016a, Myzus persicae is a highly polyphagous pest, with a host range of > 875 2016b) and M. persicae (Tatsumi and Takada, 2005; Li et al., 2007). species in 40 different plant families (Ro et al., 1998), including many Many species of parasitoids kill their host by parasitism and host economically important crops (Blackman and Eastop, 2000). Aphids not feeding (Jervis and Kidd, 1986; Heimpel and Collier, 1996), as has been only cause direct damage to crop plants by feeding on the leaves and observed in > 140 species belonging to 17 families of secreting honeydew, they also transmit > 100 plant viruses (Kennedy (Jervis and Kidd, 1986), including A. asychis (Bai and Mackauer, 1990; et al., 1962). The intensive use of insecticides to control this species has Byeon et al., 2009; Wang et al., 2016a, 2016b). Tatsumi and Takada led to populations that are now resistant to several classes of in- (2005) concluded that A. asychis would be an effective biological con- secticides, such as organophosphates (Anthon, 1955; Needham and trol agent against M. persicae. Sawicki, 1971), dimethylcarbamates and pyrethroids (Foster et al., As a commercial product, A. asychis can potentially undergo an 2002), organochlorines (Unruh et al., 1996), anthranilic diamide extensive journey (1–3 d) without feeding from the provider to the user. (Foster et al., 2012), and neonicotinoid (Nauen and Denholm, 2005; Starvation influences in different ways. Short periods of larval Slater et al., 2011; Fray et al., 2014). starvation prolonged development time and reduced larval survival,

⁎ Corresponding author. E-mail addresses: [email protected] (S.-Y. Wang), [email protected] (Y. Feng), [email protected] (N.-N. Liang), [email protected] (R. Tang), [email protected] (T.-X. Liu). https://doi.org/10.1016/j.aspen.2018.03.017 Received 17 August 2017; Received in revised form 5 March 2018; Accepted 27 March 2018 Available online 29 March 2018 1226-8615/ © 2018 Korean Society of Applied Entomology. Published by Elsevier B.V. All rights reserved. S.-Y. Wang et al. Journal of Asia-Pacific Entomology 21 (2018) 676–681 larval growth rate, pupal mass, and egg size in the butterfly Bicyclus female adults in the starvation treatments and in the control treatment anynana (Butler) (Lepidoptera: Nymphalidae) (Bauerfeind and Fischer, were recorded daily. Each starvation treatment had three replications 2008). Prolonged starvation (12 days) in 6th instar larvae caused con- and each replication had 50 female adults individually placed into a siderably lower rates of eclosion and mating, and fewer eggs were tube. There was an independent control for each starvation treatment. produced by the fall webworm, Hyphantria cunea (Drury) (Lepidoptera: Noctuidae) (Ju et al., 2008). Wang et al. (2013) found that starvation Longevity, host feeding, and reproduction prevented the development of flight muscles in mature moths of the black cutworm, Agrotis ipsilon (Rottemburg) (Lepidoptera: Noctuidae). 2nd instar M. persicae nymphs were obtained for the experiments The influences of starvation on parasitoids vary and may not always from adult aphids fed on cabbage or chili pepper plants. Chili pepper or be negative (Giron et al., 2004; Burger et al., 2005). Zang and Liu cabbage leaf discs (3 cm in diameter) were placed on top of a thin layer (2009) reported on Encarsia sophia (Girault & Dodd) that were food of water agar (1%) gel on the bottom of a plastic Petri dish (3 cm in deprived for 6 h not only killed more whiteflies via host feeding, but diameter) to keep the leaf disc fresh. To obtain 2nd instar M. persicae also lived significantly longer and parasitized more hosts than the non- nymphs, 30 M. persicae adults that had been reared on chili pepper or food deprived ones throughout their lifespan. Moreover, Zang and Liu cabbage plants were introduced into each Petri dish on the leaf disc and (2010) found that Eretmocerus melanoscutus Zolnerowich and Rose that allowed to feed and reproduce. After 24 h, these aphid adults were were food deprived for 6 h also killed significantly more whiteflies by removed and the newborn nymphs remained on the leaf disc for an- host feeding and parasitism combined than those in the control group. other 24 h. Fifty newly molted 2nd instar nymphs were included in the Detailed knowledge is lacking about the influence of starvation on experiments, and all younger nymphs and ecdyses were removed. A. asychis that occurs during transport before release. The aim of the Approximately 300 female parasitoids that had been individually present study was to better understand the effects of parasitoid star- placed into the centrifuge tubes (1 mL) were starved for 1, 2, 3, 4, or vation on subsequent host feeding and parasitism, using A. asychis as a 5 days. After the starvation treatment, the surviving female was paired biological control agent against M. persicae. with an untreated male, and both were introduced to a new Petri dish containing 50 2nd instar aphid nymphs daily until the starved female Materials and methods parasitoid adult died. After feeding and parasitizing for 24 h, both the female and male were removed, and the number of nymphs killed for Insects and plant cultures host feeding was recorded. The aphid nymphs that were not killed were retained on the leaf disc in the dish, until they developed into mummies Plants. Wheat (var. “Xinong 979”; College of Agronomy, Northwest if they were parasitized or adult aphids if they were not parasitized. The A&F University, Yangling, Shaanxi, China), cabbage (Brassica oleracea mummies were observed daily until the parasitoid adults emerged or L., Brassicaceae, var. “Qingan 80”; Institute of Vegetables and Flowers died. The following parameters were recorded: parasitoid adult long- Shanxi Academy of Agriculture Sciences Seeds, Yangling, China), and evity, aphid nymphs killed by host feeding, parasitized nymphs chili pepper (Capsicum annuum L., Solanaceae, var. “Ox horn”; Xinnong (mummified aphids), and adults emerging from the mummies. The fe- Vegetable Seeds, Inc., Hebei, China) plants were grown in 12 cm dia- male parasitoids that were not starved were included as controls. Each meter plastic pots with soil mix (peat moss: perlite = 3:1), and were starvation treatment and control treatment had 10 female parasitoids as watered and fertilized as required (Compost, COMPO Expert GmbH, replicates. Germany). These plants were enclosed in nylon cages (60 × 60 × 60 cm3), maintained in air-conditioned greenhouses and a Data analysis rearing room (25 ± 0.5 °C, 70 ± 10% RH, with a photoperiod of 14:10 LD) at the Key Laboratory of Applied Entomology, College of The longevity, numbers of nymphs on chili pepper or cabbage plants Plant Protection, Northwest A&F University, Yangling, Shaanxi pro- killed by host feeding, and parasitism by the parasitoids were analyzed vince, northwest China. Cabbage (~80 days) and chili pepper by one-way analysis of variance (ANOVA, Tukey b) and t-test (SPSS (~120 days) leaves were used in all bioassays. 22.0). To satisfy the condition of homogeneity of variance, before the Aphids. Myzus persicae and S. avenae were collected from green- one-way ANOVA (Tukey b, P < 0.05) and t-test (P < 0.05) (SPSS houses on the campus of Northwest A&F University, China in 2013. S. 22.0) were performed all percentage data (e.g., survival rate, emer- avenae was reared on wheat plants, whereas cabbage and chili pepper gence rate of mummified aphids, and percentage of female progeny) plants were used as the host plants for rearing M. persicae and for were square-root transformed ( X ), although untransformed results subsequent experiments. have been presented in all figures. To evaluate the effect of starvation Parasitoids. The parasitoid, A. asychis, was collected from the same on the control efficiency over a short time, host feeding and parasitism greenhouses as the aphids in 2013 and were reared with S. avenae as the at 3 days after starvation were analyzed. Univariate two-way ANOVA host for 11 generations in an air-conditioned rearing room (25 ± 2 °C, (Pearson correlation analysis) was applied to investigate differences in 70 ± 10% relative humidity [RH], with a photoperiod of 14:10 the longevity, numbers of nymphs killed by host feeding and parasitism, light:dark [LD]). emergence rate of mummified aphids, and percentage of female pro- geny between the plants (chili pepper and cabbage) and the starvation Starvation treatments time (1, 2, 3, 4, or 5 days) with SPSS 22.0 statistical software.

Newly emerged A. asychis female adults were collected and in- Results dividually placed into empty centrifuge tubes (1 mL) in which two small holes had been made in the tube lid and wall to maintain air Parasitoid survival after starvation circulation. A wet cotton ball was placed into each tube to supply moisture; however, no aphids or plant materials were included. The The survival rates of A. asychis female adults are shown in Fig. 1. tubes were placed into a climate controlled chamber (25 ± 0.5 °C, The survival rate declined after the parasitoids were starved for 1 day 70 ± 10% RH, with a photoperiod of 14:10 LD). The parasitoid adults and deceased sharply thereafter. Survival rate fell below 20% after in the starvation treatments were starved for 1, 2, 3, 4, 5, 6 and 7 days. 4 days starvation. In contrast, the survival rate in the control treatment After emergence, the female adults in the control group were provided did not vary significantly over the 5 days of starvation. The survival with leaf discs and 50 2nd instar M. persicae nymphs feeding on chili rates of A. asychis female adults in the starvation treatments were sig- pepper or cabbage plants daily. The numbers of surviving A. asychis nificantly lower than in the control treatments at the same time (df = 1,

677 S.-Y. Wang et al. Journal of Asia-Pacific Entomology 21 (2018) 676–681

Fig. 1. Survival rates of Aphelinus asychis female adults in starvation treatment Fig. 2. Longevity of Aphelinus asychis female adults fed and parasitized Myzus ff compared to a control. Di erent uppercase and lowercase letters represent persicae infesting chili pepper and cabbage. Different uppercase and lowercase fi ff signi cant di erence among control and all starvation treatments, respectively letters represent significant difference among control and all starvation treat- fi ff (Tukey-B, P < 0.05). *Above the bars indicate signi cant di erence between ments on chili pepper and cabbage, respectively (Tukey-B, P<0.05). control and treatment at the same starvation duration treatment (t-test, P<0.05). starvation treatments for 1 to 5 days, the number of mummified aphids on chili pepper and cabbage plants also showed a similar trend, and the 4; 1 day: P = 0.001, 2 days: P = 0.005, 3 days: P = 0.001, 4 days: lower the parasitism the longer the starvation time (df = 5, 54; on chili P = 0.001, 5 days: P < 0.001, 6 days: P < 0.001; 7 days: P < 0.001). pepper: F = 42.193, P < 0.001; on cabbage: F = 64.977, P < 0.001) (Fig. 3b). Longevity Two-way ANOVA results showed that the number of nymphs killed by A. asychis female adults by host feeding and parasitism at 3 days Two-way ANOVA results showed that the longevity of A. asychis after starvation was significantly influenced by the type of plant and fi fl female adults was signi cantly in uenced by starvation time (Table 1). starvation time (Table 1). Total numbers of aphids killed by the para- The longevity of female adults feeding on the aphids reared from the sitoids by host feeding and parasitism were not significantly different two host plants showed a similar trend, and the longevity was shorter for the two host plants; however, they showed a similar trend over the when the parasitoids were starved for longer (df = 5, 54; on chili duration of starvation, i.e., the longer the starvation duration, the less pepper: F = 20.476, P < 0.001; on cabbage: F = 14.966, P < 0.001) aphids killed (df = 5, 54; on chili pepper: F = 39.222, P < 0.001; on (Fig. 2). cabbage: F = 44.873, P<0.001) (Fig. 3c).

Aphids killed by parasitoid feeding or parasitism in 3 days after starvation Total aphids killed by the parasitoids in their entire lifespan after starvation

Two-way ANOVA results showed that the number of nymphs fed by Two-way ANOVA results showed that the host feeding, parasitizing, A. asychis females at 3 days after starvation was only significantly in- and killing number over the lifespan was significantly influenced by fluenced by starvation time (Table 1). The numbers of M. persicae killed plants and starvation time (Table 1). Total numbers of M. persicae by host feeding of the parasitoids on chili pepper and cabbage plants nymphs fed on by the parasitoids on chili pepper and cabbage plants showed a similar trend (Fig. 3a), and the numbers fed by the parasitoids showed a similar declining trend with the extended starvation time decreased over the starvation duration (df = 5, 54; on chili pepper: (df = 5, 54; on chili pepper: F = 36.335, P < 0.001; on cabbage: F = 6.108, P < 0.001; on cabbage: F = 4.392, P = 0.002) (Fig. 3a). F = 24.532, P<0.001) (Fig. 4a). Similarly, the parasitism (Fig. 4b) Two-way ANOVA results showed that the number of mummified and the total numbers of aphids fed on and parasitized during the whole aphids produced by A. asychis females at 3 days after starvation was lifespan of the parasitoids (Fig. 4c) showed a similar trend, i.e., declined significantly influenced by plants and starvation time (Table 1). After with an increase in starvation time (df = 5, 54; parasitism on chili

Table 1 The F and P values between plants and starvation duration for longevity, host feeding and parasitism.

Index Plant Starvation duration Plant × starvation duration

FPF P F P

Longevity 0.062 0.813 62.009 0.001 0.558 0.732 Feeding in 3 d 3.197 0.134 25.785 0.001 0.385 0.858 Parasitism in 3 d 41.505 0.001 269.140 0.001 0.376 0.864 Killing in 3 d 42.261 0.001 234.500 0.001 0.356 0.878 Feeding in lifespan 7.463 0.041 239.340 0.001 0.245 0.941 Parasitism in lifespan 10.609 0.023 348.821 0.001 0.522 0.759 Killing in lifespan 12.883 0.016 421.349 0.001 0.399 0.849 Emergence rate 4.747 0.081 12.553 0.007 0.700 0.624 Female progeny 14.095 0.013 424.454 0.001 0.388 0.856 Female proportion 0.302 0.607 3.859 0.082 0.827 0.533

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Fig. 4. Total numbers of 2nd instar Myzus persicae nymphs killed by Aphelinus Fig. 3. Number of aphids killed by Aphelinus asychis female adults through host asychis by host feeding (a), parasitism (b), and total aphids killed (c) in the feeding (a), parasitism (b) and total aphids killed (c) in three days after star- parasitoid's lifespan after starvation treatment in life span. Different uppercase vation treatment. Different uppercase and lowercase letters represent sig- and lowercase letters represent significant difference among control and all nificant difference among control and all starvation treatments on chili pepper starvation treatments on chili pepper or cabbage, respectively (Tukey-B, or cabbage, respectively (Tukey-B, P < 0.05). *Above the bars indicate sig- P<0.05). nificant difference between chili pepper and cabbage at the same starvation duration treatment (t-test, P<0.05). mummies was only significantly influenced by starvation time (Table 1). The starvation treatment affected the number of parasitoids pepper: F = 104.521, P < 0.001; parasitism on cabbage: F = 79.507, emerging from aphid mummies, slightly lower rates of emergence oc- P < 0.001; total numbers killed on chili pepper: F = 98.730, curred for parasitoids that were starved for a longer duration than those P<0.001; total numbers of aphids killed on cabbage: F = 71.825, starved for a shorter duration both on chili pepper and cabbage plants P < 0.001). (df = 5, 54; on chili pepper: F = 3.060, P = 0.017; on cabbage: F = 6.195, P < 0.001) (Fig. 5a). Emergence and female progeny Two-way ANOVA results showed that the number of female pro- genies was significantly influenced by plants and starvation time; Two-way ANOVA results showed that the emergence rate of aphid however, only starvation duration significantly affected the proportion

679 S.-Y. Wang et al. Journal of Asia-Pacific Entomology 21 (2018) 676–681

Discussion

Food is an important biological factor for survival. In natural en- vironments, shortage of food causes an ageing phenomenon (Chen et al., 2010). The relationship between the tolerance of starvation and population development of natural enemies is closely related. Starva- tion negatively affects growth, development, and reproduction in in- sects, and leads to organ failure and death due to the shortage of nu- trients in the body (Chen et al., 2000). Insect species vary greatly in their ability to withstand starvation. In the present study, the absolute survival rate of A. asychis female adults suffering from starvation de- creased significantly. Without any prey and water, the gravid female mite, Neoseiulus californicus (McGregor), survived for 4.3 days (Toyoshima et al., 2009). Short-term starvation during the 2nd instar larval stage had no significant effects on survival but it shortened the longevity in the fourth and 6th instar larvae of H. cunea (Ju et al., 2008). The survival rate of a mealybug Phenacoccus solenopsis (Tinsley) female adult decreased approximately by 50% after starving for 8 days (Zheng et al., 2011). The effect of starvation on insects not only influences survival but also longevity. The starvation treatment in the present study shortened the longevity of A. asychis females feeding on M. persicae nymphs both on chili pepper and cabbage plants. Momen (1994) reported that the duration of food deprivation affected the longevity of the mite Am- blyseius barkeri (Hughes) and Zheng et al. (2011) found that the long- evity of a female mealybug P. solenopsis female was lower when ex- posed to short periods (4 days) of starvation. These results are similar to those found in the present study. The emergence rate of parasitoids from mummified aphids was not affected by the duration of starvation; however, the total number of female progeny produced fell sharply with increasing starvation time. Numbers emerging after 5 d of starvation were 20% lower than that in the control. In turn, this would affect the parasitoid population, and thus their ability to control aphids. At the time of release to the greenhouse or field, the density of pests is generally low and the natural enemy might face starvation. Therefore, the fecundity of natural ene- mies under starvation conditions is limited by natural environments. In our research, the number of mummified aphids produced by A. asychis female adults of 2nd instar M. persicae nymphs feeding on chili pepper or cabbage plants decreased significantly as the starvation duration increased. Fecundity of A. asychis females was thus seriously affected by starvation. Momen (1994) showed a significant decline in total ovipo- sition when female adult mites experienced food deprivation. Ju et al. (2008) reported that the number of eggs produced by H. cunea starved for 12 days decreased significantly. However, the effect of starvation on different insect species varies. With a short period of starvation (4 days), there was no significant difference in oviposition between the starved and feeding female mealybugs (Zheng et al., 2011). The emergence rate also affected the population continuation and expan- Fig. 5. Emergence rate of mummified aphids (a), total number (b) and per- sion. In the present study, when the parasitoids were starved for 1 to centage (c) of female progeny produced by Aphelinus asychis after starvation 5 days, the emergence rate of mummified aphids produced by the treatments. Different uppercase and lowercase letters represent the significant parasitoid females decreased from 93% to 89%, which demonstrated difference among the control and all starvation treatments on chili pepper or that the influence of starvation on the parents might be inherited by the cabbage, respectively (Tukey-B, P<0.05). next generation, and thus affect the development of progeny. In our research, after starvation treatment for 1 to 5 days the per- of female progenies (Table 1). Starvation duration significantly reduced centage of female progeny decreased from 84% to 80%. The progeny the numbers of female progeny produced (Fig. 5b) (df = 5, 54; on chili produced by unmated A. asychis females were male and a higher pro- pepper: F = 82.937, P < 0.001; on cabbage: F = 82.082; P < 0.001). portion of males might increase the chance of mating and copulation for The percentage of female progeny produced by the parasitoids was si- females, which would enhance the percentage of mated female adults milar among different host plant or starvation duration treatments, and produce more female progeny. We speculated that this change in except for the 5 days starvation treatment that significantly reduced the the sex ratio might be a compensation mechanism to avoid population percentage of female progeny on cabbage plants (df = 5, 54; F = 4.803, decrease. Similar to our research, the sex ratio of progeny produced by P < 0.05) (Fig. 5c). A. barkeri females changed from 1.1 female: 1 male under mild food shortage to 1 female: 1.5 males under severe food deprivation (Momen, 1994). Moreover, we found that the numbers of female progeny de- creased when the starvation duration increased, which suggests that the

680 S.-Y. Wang et al. Journal of Asia-Pacific Entomology 21 (2018) 676–681 starvation treatment caused negative effects on population growth. killing caused by Aphelinus asychis (Hymenoptera: Aphelinidae), a parasitoid of According to the hormesis theory, weak stimulation is beneficial for cotton aphid, (Homoptera: Aphididae). J. Fac. Agric. Kyushu Univ. 54, 369–372. an organism; however, strong stimulation results in inhibition Chen, J.M., Yu, X.P., Lv, Z.X., Zheng, X.S., 2000. Hunger tolerance of Microvelia horvathi (Arumugam et al., 2006). The influence of food deprivation before re- hibernating generation. Chin. J. Appl. Ecol. 11, 609–611. lease on host feeding and the fitness of the parasitoids have received Chen, H.F., Huang, S.S., Zhang, Y.Z., Zeng, X., Huang, Z.H., 2010. Control efficacy of Trichogramma japonicum against Chilo suppressalis and Chilaraea auricilia. Chin. J. attention during the past decade. Zang and Liu (2009) demonstrated Appl. Ecol. 21, 743–748. that En. sophia (Girault and Dodd) that were food deprived for 6 h not van Emden, H.F., Harrington, R., 2007. Aphids as Crop Pests. CABI, Wallingford, only killed more whiteflies via host feeding, but also lived significantly Oxfordshire, UK. longer and parasitized more hosts than those that were not food de- Foster, S.P., Denholm, I., Devonshire, A.L., 2002. Field-simulator studies of insecticide resistance to dimethylcarbamates and pyrethroids conferred by metabolic and target prived. In another study, Zang and Liu (2010) concluded that the effect site-based mechanisms in peach-potato aphids, Myzus persicae (Hemiptera: of Eretmocerus melanoscutus on controlling whitefly nymphs in the short Aphididae). Pest Manag. Sci. 58, 811–816. Foster, S.P., Denholm, I., Rison, J.L., Portillo, H.E., Margaritopoulis, J., Slater, R., 2012. term and for their entire lifespan could be improved if they were fi fi Susceptibility of standard clones and European eld populations of the green peach starved for 6 h prior to release. In contrast to these ndings, Luo and aphid, Myzus persicae, and the cotton aphid, Aphis gossypii (Hemiptera: Aphididae), to Zhong (2012) found that the predation numbers of Neoseiulus barkeri the novel anthranilic diamide insecticide cyantraniliprole. Pest Manag. Sci. 68, – (Hughes) and Euseius nicholsi (Ehara et Lee) reached a peak 4 h after 629 633. Fray, L.M., Leather, S.R., Powell, G., Slater, R., McIndoe, E., Lind, R.J., 2014. Behavioural starvation treatment, and then gradually decreased to a steady level, avoidance and enhanced dispersal in neonicotinoid-resistant Myzus persicae (Sulzer). which was approximately equal to the control group. In the present Pest Manag. 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