Lethal and sublethal effects of dinotefuran on two

Journal of Asia-Pacific Entomology 20 (2017) 325–330

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Lethal and sublethal effects of dinotefuran on two invasive whiteflies, Bemisia tabaci (Hemiptera: Aleyrodidae) Cheng Qu a,1, Wei Zhang a,1, Fengqi Li a, Guillaume Tetreau b, Chen Luo a, Ran Wang a,⁎ a b

Institute of Plant and Environment Protection, Beijing Academy of Agriculture and Forestry Sciences, Beijing 100097, China Univ. Perpignan Via Domitia, IHPE UMR 5244, CNRS, IFREMER, Univ. Montpellier, F-66860 Perpignan, France

a r t i c l e

i n f o

Article history: Received 15 November 2016 Revised 4 February 2017 Accepted 8 February 2017 Available online 9 February 2017 Keywords: Bemisia tabaci Neonicotinoid Dinotefuran Toxicity Sublethal effects

a b s t r a c t Two invasive whitefly cryptic species, Middle East-Asia Minor 1 (MEAM1) and Mediterranean (MED), are the most invasive and notorious pests on diverse crops and have significantly impacted agricultural production systems globally. This circumstance emphasizes the need for a better approach for controlling these species. In this study, the lethal effect of six insecticides and the sublethal effects of dinotefuran on B. tabaci MEAM1 and MED were examined. Among the six insecticides tested, dinotefuran was the most toxic to both B. tabaci MEAM1 and MED adults with LC50 values of 5.54 mg/L and 6.01 mg/L, respectively. After treating adults of the two important species with LC25 of 1.70 mg/L (MEAM1) and 2.12 mg/L (MED), the transgenerational effects of dinotefuran on survival, developmental duration, and fecundity of F1 generation of B. tabaci MEAM1 and MED adults were observed respectively, which increased the developmental time and decreased survival rates of nymph, pseudopupa and adult. The fecundity of tested females was also reduced markedly. In summary, these results indicate that dinotefuran could be one excellent candidate that may effectively control two invasive whitefly populations. © 2017 Published by Elsevier B.V. on behalf of Korean Society of Applied Entomology, Taiwan Entomological Society and Malaysian Plant Protection Society.

Introduction The tobacco whitefly Bemisia tabaci (Gennadius) is now considered as a complex of genetically differentiating cryptic species that is one of the most notorious globally agricultural pests. B. tabaci damages plants directly by stylet probing and indirectly by acting as a vector for begomoviruses (De Barro et al., 2011). At present, the Middle EastAsia Minor1 (MEAM1 or biotype B) and the Mediterranean (MED or biotype Q) species are badly invasive and have brought about considerable economic loss to a lot of important field, vegetables, and ornamental crops. The MEAM1 was initially reported in China in the mid-1990s (Chen, 1997), then it replaced the native whitefly species rapidly and became the dominant whitefly in both greenhouse and field crops (Luo et al., 2002). In 2003, MED was first detected in Yunnan province of China (Chu et al., 2006), and then replaced MEAM1 as the dominant whitefly in China from 2007 (Pan et al., 2011). At present, the use of chemical pesticides is the most important way to control B. tabaci MEAM1 and MED in many agricultural crops throughout the world. Due to the heavy dependence on and overuse of chemical insecticides for the control of B. tabaci, many whitefly populations have developed resistance to conventional insecticides such as organophosphates, ⁎ Corresponding author. E-mail address: [email protected] (R. Wang). 1 These authors contributed equally to this work.

insect growth regulators and pyrethroids (Ahmad et al., 2002; Nauen et al., 2002; Basit et al., 2013; Zheng et al., 2017). Therefore, massive and extensive application of above mentioned insecticides is not a suitable choice for conducting agricultural production with low insecticide residues. Neonicotinoids are agonists of acetylcholine that selectively act on nicotinic acetylcholine receptor (nAChR) in the central nervous system of insects. They have become one of the most important chemical classes of insecticides owing to the favorable toxicological properties, broad control spectrum, and multifarious application methods (Bass et al., 2015). A series of commercialized neonicotinoids have been applied in N120 countries and are particularly active for the control of hemipteran pests (Nauen et al., 2008), and a number of lepidopteran, dipteran and coleopteran pest species as well (Jeschke et al., 2011). Apart from killing the target pests directly, numerous cases of sublethal effects of neonicotinoids on the biology and physiology of a variety of target insects have been evidenced (Tan et al., 2012; Qu et al., 2015; Lu et al., 2016; Wang et al., 2016). Nevertheless, the advantages of neonicotinoids were seriously threatened because of the evolution of resistance, and as a result, failures to control pests with some earlier neonicotinoids at recommended or standard dosage have been increasingly reported (Bass et al., 2015). The application of higher doses of insecticides will lead to an increase in the amount of insecticide residues in the environment and therefore endanger non-target organisms such as bees, birds, and mammals (Fairbrother et al., 2014).

http://dx.doi.org/10.1016/j.aspen.2017.02.006 1226-8615/© 2017 Published by Elsevier B.V. on behalf of Korean Society of Applied Entomology, Taiwan Entomological Society and Malaysian Plant Protection Society.

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C. Qu et al. / Journal of Asia-Pacific Entomology 20 (2017) 325–330

Over the past decades of pest control with the high dependence on insecticides, B. tabaci has developed resistance to many conventional insecticides so rapidly that the use of conventional insecticides which were previously highly effective for the control of them has become less effective method in pest management (Palumbo et al., 2001). In China, the extensive application of insecticides in the field has increased the number of reported cases on the resistance of B. tabaci to various classes of insecticides, such as organophosphates, carbamates, pyrethroids, and earlier neonicotinoids, which used to be highly effective against whiteflies (Ma et al., 2007; Luo et al., 2010; Wang et al., 2010; Yuan et al., 2012). For example, Imidacloprid was the first neonicotinoid commercialized in 1991, and then others such as nitenpyram, acetamiprid, thiamethoxam, and thiacloprid were developed and globally employed for controlling sucking pests (Bass et al., 2015). Unfortunately, the first case of neonicotinoid resistance was reported after about five years in 1996, with a significant reduction in the efficacy of imidacloprid in B. tabaci continuously treated with neonicotinoids (Cahill et al., 1996). In China, both MEAM1 and MED have developed resistance to various classes of insecticide and, among them, resistance to several earlier neonicotinoids has been widely reported from many geographic areas (Ma et al., 2007; Luo et al., 2010; Wang et al., 2010; Yuan et al., 2012). Dinotefuran is a 3rd-generation neonicotinoid and has been proved to be efficient for controlling several different insect pests (Bouhsira et al., 2012; Arthur and Fontenot, 2013; de Oliveira et al., 2015). More importantly, it could be a potentially good candidate for mitigating the resistance development in B. tabaci because the molecular mechanisms of metabolic resistance to this insecticide have been shown to differ from those of most other neonicotinoids such as imidacloprid (Meng et al., 2016). Apart from directly inducing mortality, sublethal effects of dinotefuran have been reported on several insect pests (Bao et al., 2009; Shi et al., 2011; Miao et al., 2014). Specifically speaking, the sublethal concentrations could affect important fitness parameters of insect pests such delaying the developmental duration and decreasing the fecundity of the F1 generation, and it has been proved that many insecticides such as imidacloprid, bifenthrin, buprofezin, and cycloxaprid could exert sublethal effects on B. tabaci (Sohrabi et al., 2012; He et al., 2013; Wang et al., 2016). Here, we investigated the lethal effect of dinotefuran on the adult B. tabaci MEAM1 and MED, and compared the toxicological activities with five other successfully commercial insecticides in the laboratory. Moreover, we evaluated the sublethal effects of dinotefuran on the development, fecundity and oviposition period of B. tabaci MEAM1 and MED adults, and on hatchability of the eggs. Materials and methods Insects Laboratory strain of B. tabaci MEAM1 was originally sampled from a cabbage field (Brassica oleracea var. Jingfeng 1) in Beijing in 2004, and then maintained on cotton plants (Gossypium hirsutum L. var. ‘Shiyuan 321’) in a glasshouse. Laboratory strain of B. tabaci MED was originally collected from poinsettia (Euphorbia pulcherrima) in Beijing in 2008 and subsequently maintained on cotton plants (Gossypium hirsutum L. var. ‘Shiyuan 321’) in another separated glasshouse. The two strains without exposed to any insecticide were maintained under a 16:8 h (L:D) photoperiod at 27 ± 1 °C and 60 ± 10% humidity. All adults tested in bioassays were b7-days-old and both females and males were used at a sex ratio of 1:1. Insecticides and chemicals All insecticides used were technical grade with purity higher than 94%. Dinotefuran (98%) was obtained from Jiangsu Kesheng Group Co.

(Jiangsu, China) and thiamethoxam (97%) were obtained from Hebei Brilliant Chemical Co., Ltd. (Hebei, China). Bifenthrin (97%) and betacypermethrin (95%) were obtained from Guangdong Liwei Chemical Industry Co., Ltd. (Guangdong, China). Chlorpyrifos (95%) was obtained from Jiangsu Kinhon Chemical Co., Ltd. (Jiangsu, China). Acetone was purchased from Beijing Chemical Reagent Co., Ltd. (Beijing, China). Lethal effects of the six insecticides on B. tabaci MEAM1 and MED The lethal effects of dinotefuran, imidacloprid, thiamethoxam, bifenthrin, beta-cypermethrin, and chlorpyrifos to B. tabaci MEAM1 and MED adults were determined using a leaf dipping bioassay procedure, as previously described by Wang et al. (2016). All insecticide stock solutions tested were prepared in acetone, and then diluted in distilled water containing Triton X-100 (0.1‰) to obtain the working concentrations. Leaf discs (22 mm diameter) from cotton plants were dipped for 20s in the insecticide solution or in distilled water containing 0.1‰ triton X-100 as a control. After leaf discs were air dried, they were placed in a flat-bottom glass tube (78 mm long) containing 2 mL agar (15 g/L) with their adaxial surface downward on the agar. Adult whiteflies were collected into these tubes by inverting the tubes over the insects that were maintained on cotton plants in a greenhouse and allowing them to fly into the tubes. After randomly collecting 20–30 adults, the open and of each tube was sealed with a cotton plug. All the tubes were maintained in an incubator at 27 ± 1 °C with a 16:8 h (L:D) photoperiod and 60 ± 10% relative humidity (RH). Mortality was evaluated after 48 h and immobile adults were considered as dead. For each bioassay, there were six working concentrations with four replicates tubes per each concentration and specifically working concentrations of six tested insecticides were shown in the supplementary materials (Table S1). Sublethal effects of dinotefuran on B. tabaci MEAM1 and MED Based on the results of mortality for dinotefuran B. tabaci MEAM1 and MED adults were exposed to respective sublethal concentration (LC25 value of 1.70 mg/L and 2.12 mg/L, respectively) of dinotefuran for 48 h using the same leaf dipping method as used in the bioassay for mortality. The following fitness endpoints on F1 generations of B. tabaci MEAM1 and MED were monitored: survival rate and developmental duration of the nymphs, pseudopupae and adults, fecundity, oviposition duration and hatchability of eggs of the next generation. Briefly, a total of 20 insect-free host plants were randomly placed in four separate insect-proof cages (five plants per each cage). Two of four cages were subjected to the treatment of LC25 of dinotefuran for MEAM1 and MED, respectively, while the remaining two cages were served as the control for MEAM1 and MED, respectively. Then, 100 adults of B. tabaci MEAM1 or MED that previously fed on dinotefuran treated (LC25) cotton leaves by leaf dipping method (Wang et al., 2016) were added to the treatment cages for oviposition. As control, the same numbers of untreated B. tabaci MEAM1 or MED adults were introduced into the each control cage. After 12 h allowance for oviposition, the plants were removed from the cages and then two leaves each per plant (10 leaves in total per cage) were randomly selected and marked with a marker pen. These selected ten leaves from each cage were assigned to control group and treatment group for MEAM1 and MED, respectively. The eggs on the unselected leaves were removed by observation under a microscope. Twenty eggs were left on each selected leaf and the abaxial surface of the selected leaves was sketched and the position of each egg was marked. These drawings allowed us to follow each whitefly egg until adult emergence. The plants were then placed in a separate climatic chamber at 27 ± 1 °C, 60 ± 10% RH and a 16:8 h (L:D) photoperiod. When pseudopupae were checked on a specific leaf, pseudopupae and leaf were contained in a leaf clip-cage (one clip-cage per leaf), and the numbers and adults on each plant were counted and recorded daily. After newly emerged adults emerged,


each one was transferred to a new leaf with a clip-cage for oviposition. After 24 h, the adults were moved to new leaf with a clip-cage, the leaves with eggs were cut down and the fecundity was recorded until the death of all individuals. Hatchability of the eggs was recorded by monitoring and counting daily until the eggs developed into 1st-instar nymphs. Statistical analysis Lethal concentrations for 50% of B. tabaci MEAM1 and MED adults to six tested insecticides (LC50) were calculated by Probit regression using LeOra Software (2002). LC25 were also calculated for dinotefuran following the same method. The resistance factor (RF) was calculated by dividing the estimated LC50 of MED by the estimated LC50 of MEAM1 populations for each insecticide following Robertson and Preisler method (Robertson and Preisler, 1992). All data were checked for normality using non-parametric Kolmogorov-Smirnov tests (P b 0.05). Data showing a normal distribution (survival rate, oviposition duration, fecundity and hatchability) were compared using Student's t-test (P b 0.05). For data that were not normally distributed (developmental duration), direct estimates were compared using the nonparametric Mann-Whitney U test (P b 0.05). Comparisons were made between the control (CK) and LC25 treatment (MEAM1 or MED). All statistical analyses were conducted using the SPSS (2011) software. Results Lethal effects of six insecticides on B. tabaci MEAM1 and MED adults The LC50 values of the six insecticides against B. tabaci MEAM1 and MED adults fed on leaves dipped in each of the insecticides at different concentrations for 48 h are listed in Table 1. The mortality rate in the control was b 5%. The highest toxicity for MEAM1 and MED was exerted by dinotefuran (5.54 mg/L and 6.01 mg/L of LC50 for MEAM1 and MED, respectively) followed by imidacloprid (9.74 mg/L and 20.37 mg/L of LC50, respectively), thiamethoxam (8.77 mg/L and 24.26 mg/L of LC50, respectively), bifenthrin (25.97 mg/L and 104.60 mg/L of LC50, respectively), chlorpyrifos (390.94 mg/L and 930.34 mg/L of LC50, respectively) and beta-cypermethrin (420.16 mg/L and 1184.67 mg/L of LC50, respectively). The toxicity of the six insecticides tested on B. tabaci adults was ranked as dinotefuran N imidacloprid N thiamethoxam N bifenthrin N chlorpyrifos N beta-cypermethrin. Moreover, in the 6 insecticides, compare with the MEAM1, the MED showed relatively lower susceptibility with higher LC50 to each tested insecticide (Table 1). Also, resistance factor (RF) indicated that the MED shows higher resistance than the MEAM1 in all tested insecticides and only the RF of dinotefuran exhibits no significant difference between MEAM1 and MED (Table 1).

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Sublethal effects of dinotefuran for B. tabaci MEAM1 and MED In this study, B. tabaci MEAM1 and MED adults were exposed to sublethal level of dinotefuran since insecticides are usually degraded gradually in the field (Desneux et al., 2007) after their initial application, which in turn may lower their exposure levels to sublethal concentrations. Bioassay results of dinotefuran showed that the LC25 values of dinotefuran to B. tabaci MEAM1 and MED were 1.70 mg/L and 2.12 mg/L, respectively. After the exposure to the specific sublethal concentration of dinotefuran, fitness endpoints such as developmental duration, survival rate and fecundity per female of B. tabaci MEAM1 and MED were altered significantly when compared to the respective controls. For B. tabaci MEAM1, the development duration from egg to 2nd stage of nymph was 10.05 days which was significantly longer than the control (9.72 days, P b 0.0001) (Table 2). The survival rates of 2nd instar nymph, pseudopupa, and adult of B. tabaci MEAM1 after LC25 treatment significantly decreased by 9.81–11.14% when compared to the control (t = 3.832, df = 18, P = 0.001; t = 3.534, df = 18, P = 0.002; t = 4.225, df = 18, P = 0.001, respectively) (Table 2). However, no significant difference was observed between control and treatment in the survival rate of 3rd instar (t = −1.29, df = 18, P = 0.213). Moreover, fecundity of the treated group of MEAM1 (112.47 ± 3.37) was significantly lower than that of the control (136.07 ± 4.89) (t = 3.591, df = 28, P = 0.001) (Fig. 1A). For B. tabaci MED, the developmental durations from egg to 3rd instar, pseudopupa and adult in the treatment were 13.22, 17.72, and 21.36 days, which were significantly 0.52, 1.69, and 0.79 days longer than those in the controls, respectively (P b 0.0001). The survival rate of pseudopupa (84.82 ± 1.94%) and adults (83.39 ± 1.92%) of B. tabaci MED in the treatment group significantly decreased by 12.10–12.82% when compared to the control (96.92 ± 1.12% and 96.21 ± 1.12%, respectively) (t = 5.395, df = 18, P b 0.0001; t = 5.762, df = 18, P b 0.0001, respectively). Furthermore, similar to MEAM1, fecundity of adult MED in the treatment (129.67 ± 7.30) was significantly lower than the control (153.47 ± 5.54) (t = 2.596, df = 28, P = 0.015) (Fig. 1D). Discussion Our study proved that the lethal effect of dinotefuran was the highest among the six insecticides tested against B. tabaci MEAM1 and MED, while imidacloprid, thiamethoxam, and bifenthrin exhibited moderate to relatively high efficacy and chlorpyrifos and betacypermethrin displayed low toxicity. Unlike the other tested insecticides, according to the RF values, lethal effect of dinotefuran showed no significant difference for B. tabaci MEAM1 and MED which means dinotefuran could be employed to control the two important cryptic species simultaneously like cycloxaprid, a novel cis-nitromethylene neonicotinoid insecticide (Wang et al., 2016). The results also revealed that exposure to sublethal concentration (LC25) of dinotefuran could

Table 1 Median lethal concentration (LC50) of the six different insecticides on B. tabaci MEAM1 and MED. Insecticides

Cryptic species

Number

Slope ± SE

LC50 (mg/L)

LC50 (95% FL) (mg/L)a

X2 (df)

P values

RF (95% FL)b

Dinotefuran

MEAM1 MED MEAM1 MED MEAM1 MED MEAM1 MED MEAM1 MED MEAM1 MED

646 667 651 649 655 661 666 632 660 682 683 642

1.31 1.49 1.17 1.04 1.08 1.01 1.30 1.22 1.03 1.01 1.14 1.23

5.54 6.01 9.74 20.37 8.77 24.26 25.97 104.60 420.16 1184.67 390.94 930.34

4.51–6.69 5.05–7.08 7.65–12.01 16.26–25.75 7.04–10.92 19.28–31.12 21.39–31.18 85.76–129.76 303.53–593.66 942.00–1536.56 288.87–535.22 764.60–1146.58

3.41 (4) 3.32 (4) 2.07 (4) 1.02 (4) 3.30 (4) 3.01 (4) 3.86 (4) 3.66 (4) 4.05 (4) 3.81 (4) 4.29 (4) 3.94 (4)

0.45 0.48 0.76 0.90 0.56 0.57 0.39 0.49 0.42 0.41 0.35 0.51

1.08 (0.85–1.42) 2.09 (1.48–2.88) 2.77 (2.18–4.37) 4.03 (3.04–5.34) 2.82 (2.02–3.94) 2.38 (1.78–3.18)

Imidacloprid Thiamethoxam Bifenthrin Beta-cypermethrin Chlorpyrifos a b

± ± ± ± ± ± ± ± ± ± ± ±

0.11 0.12 0.11 0.11 0.11 0.10 0.11 0.11 0.10 0.10 0.11 0.11

Concentration of insecticide killing 50% of adults and its 95% fiducial limits. RF = resistance factor, calculated between the estimated LC50 of MED and MEAM1 populations through Robertson and Preisler (1992) method.

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Table 2 Sublethal effects of dinotefuran on development time and survival in specific stage of B. tabaci F1 generations MEAM1 and MED (mean ± SE). Fitness endpoints

1st instar

MEAM1 cryptic species Development duration from egg to specific stage (days) Control 6.55 ± 0.04 Dinotefuran 6.59 ± 0.05 Survival (%) Control Dinotefuran MED cryptic species Development duration from egg to specific stage (days) Control 6.75 ± 0.05 Dinotefuran 6.70 ± 0.04 Survival (%) Control Dinotefuran

2nd instar

3rd instar

Pseudopupa

Adult

9.72 ± 0.06 10.05 ± 0.11*

12.80 ± 0.09 12.94 ± 0.08

15.68 ± 0.08 15.77 ± 0.08

19.35 ± 0.09 19.46 ± 0.09

98.00 ± 0.82 86.86 ± 2.79*

88.39 ± 2.21 92.13 ± 1.87

96.67 ± 1.23 86.86 ± 2.49*

95.92 ± 1.53 84.85 ± 2.13*

10.23 ± 0.07 10.47 ± 0.07

12.70 ± 0.11 13.22 ± 0.09*

16.03 ± 0.10 17.72 ± 0.09*

20.57 ± 0.10 21.36 ± 0.12*

98.50 ± 1.07 95.50 ± 1.38

94.86 ± 1.71 92.65 ± 1.59

96.92 ± 1.12 84.82 ± 1.94*

96.21 ± 1.12 83.39 ± 1.92*

Comparisons are made between the control and the LC25 treatment. Means in the same column and marked with * are significantly different at the P b 0.05 level according to the nonparametric Mann-Whitney U tests.

give rise to significant physiological and developmental effects on B. tabaci adults and nymphs, which could contribute to the management of B. tabaci MEAM1 and MED. Furthermore, compare with imidacloprid, one of the most successfully commercialized insecticide, which showed negative effects against many organisms (Tisler et al., 2009; Brandt et al., 2016; Lonare et al., 2016). Previous studies on toxicity and ecotoxicity of dinotefuran have indicated that dinotefuran has a fairly low toxicity to mammals, avian species, aquatic organisms, and natural environment (Wakita et al., 2005; Wakita, 2011). Our study indicated high susceptibility of both MEAM1 and MED to dinotefuran in the lab, which suggested that dinotefuran, with the diverse mechanism of resistance from other earlier neonicotinoids in whitefly (Meng et al., 2016), would be a promising alternative for the targeted control of B. tabaci MEAM1 and MED.

Many studies have shown that sublethal effects on the development and fecundity of insect depended on the species studied and on the class of insecticide applied (Desneux et al., 2007). In several cases, sublethal doses exerted significant effects on arthropods by shortening egg-laying duration, reducing fecundity, and decreasing egg hatching rate (Tan et al., 2012; Lu et al., 2016; Wang et al., 2016; Xu et al., 2016). For instance, low concentrations (LC10 and LC25) of cyantraniliprole significantly prolonged developmental duration of eggs and nymphs of B. tabaci with markedly negative impact on fecundity and hatching rate of next-generation eggs (Wang et al., 2017). In Nilaparvata lugens (Stål), sublethal concentration of dinotefuran significantly reduced copulation rate and fecundity after exposure to LC20 concentration (Bao et al., 2009). Occasionally, sublethal concentrations of insecticides could have positive effects on arthropods (Kerns and Stewart, 2000; Guedes

Fig. 1. Sublethal effects of dinotefuran (LC25) on fecundity per female, oviposition duration, and egg hatching rate of F1 generations of B. tabaci MEAM1 (A, B, and C, respectively) and of B. tabaci MED (D, E, and F, respectively). CK indicates control and * indicate significant differences when compared to each control (P b 0.05).


and Cutler, 2014). For example, Yu et al. (2010) reported that low concentrations of imidacloprid stimulated the fecundity of green peach aphid. Similarly, insecticide-induced hormesis in Oligonychus ilicis (McGregor), Aphis glycines (Matsumura) and Myzus persicae (Sulzer) could stimulate reproduction and therefore could lead to an increase in their population size (Cutler et al., 2009; Cordeiro et al., 2013; Qu et al., 2015). Similar finding was reported in Plutella xylostella in which low concentrations of beta-cypermethrin could stimulate their population growth by affecting the survival rate, population growth rate, and fecundity (Han et al., 2011). In addition to the effects on biology and physiology of arthropods, sublethal concentrations may also affect the behavior of insects (Desneux et al., 2007). Numerous studies have reported positive and negative sublethal effects of insecticides on orientation behaviors of insects (Komeza et al., 2001; Desneux et al., 2004; Delpuech et al., 2005). Besides, using electrical penetration graphing (EPG), significant sublethal effects of several neonicotinoids on feeding behavior have been observed in several insects including Sitobion avenae (Fabricius) and Rhopalosiphum padi (Linnaeus) (Daniels et al., 2009; Cui et al., 2012; Miao et al., 2014). Miao et al. (2014) pointed out that low concentration of dinotefuran could significantly alter the feeding behavior of S. avenae in several aspects such as the duration of the non-probing periods and the time of ingestion in xylem. It is possible that dinotefuran could impact the feeding behavior of B. tabaci that may also be contributed to protect agricultural crops against the attack by the whiteflies and the subsequent transfer of disease-causing viruses and bacteria. Hence, these behavioral parameters affected by sublethal effects need further investigation. Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.aspen.2017.02.006. Acknowledgements This work was supported partly by research grants from the National Key Research and Development Program of China (2016YFD0201000) and the earmarked fund for Beijing Leafy Vegetables Innovation Team of Modern Agro-industry Technology Research System (blvt-13). References Ahmad, M., Arif, M.I., Ahmad, Z., Denholm, I., 2002. Cotton whitefly (Bemisia tabaci) resistance to organophosphate and pyrethroid insecticides in Pakistan. Pest Manag. Sci. 58, 203–208. Arthur, F.H., Fontenot, E.A., 2013. Efficacy of dinotefuran (Alpine® spray and dust) on six species of stored product insects. J. Stored Prod. Res. 55, 55–61. Bao, H.B., Liu, S.H., Gu, J.H., Wang, X.Z., Liang, X.L., Liu, Z.W., 2009. Sublethal effects of four insecticides on the reproduction and wing formation of brown planthopper, Nilaparvata lugens. Pest Manag. Sci. 65, 170–174. Basit, M., Saeed, S., Ahmad, M., Sayyed, A.H., 2013. Can resistance in Bemisia tabaci (Homoptera: Aleyrodidae) be overcome with mixtures of neonicotinoids and insect growth regulators? Crop. Prot. 44, 135–141. Bass, C., Denholm, I., Williamson, M.S., Nauen, R., 2015. The global status of insect resistance to neonicotinoid insecticides. Pestic. Biochem. Physiol. 121, 78–87. Bouhsira, E., Lienard, E., Jacquiet, P., Warin, S., Kaltsatos, V., Baduel, L., Franc, M., 2012. Efficacy of permethrin, dinotefuran and pyriproxyfen on adult fleas, flea eggs collection, and flea egg development following transplantation of mature female fleas (Ctenocephalides felis felis) from cats to dogs. Vet. Parasitol. 190, 541–546. Brandt, A., Gorenflo, A., Siede, R., Meixner, M., Büchler, R., 2016. The neonicotinoids thiacloprid, imidacloprid, and clothianidin affect the immunocompetence of honey bees (Apis mellifera L.). J. Insect Physiol. 86, 40–47. Cahill, M., Gorman, K., Day, S., Denholm, I., Elbert, A., Nauen, R., 1996. Baseline determination and detection of resistance to imidacloprid in Bemisia tabaci. Bull. Entomol. Res. 86, 343–349. Chen, L.G., 1997. The damage and morphological variations of Bemisia tabaci (Gennadius) on ornamental plants. J. Shanghai Agric. College 15, 186–189. Chu, D., Zhang, Y.J., Brown, J.K., Cong, B., Xu, B.Y., Wu, Q.J., Zhu, G.R., 2006. The introduction of the exotic Q biotype of Bemisia tabaci from the Mediterranean region into China on ornamental crops. Fla. Entomol. 89, 168–174. Cordeiro, E.M.G., de Moura, I.L.T., Fadini, M.A.M., Guedes, R.N.C., 2013. Beyond selectivity: are behavioral avoidance and hormesis likely causes of pyrethroid-induced outbreaks of the southern red mite Oligonychus ilicis? Chemosphere 93, 1111–1116. Cui, L., Sun, L.N., Yang, D.B., Yan, X.J., Yuan, H.Z., 2012. Effects of cycloxaprid, a novel cisnitromethylene neonicotinoid insecticide, on the feeding behaviour of Sitobion avenae. Pest Manag. Sci. 68, 1484–1491.

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