Sublethal effects of imidacloprid on the performance of the bird cherry-oat aphid Rhopalosiphum padi

Wenqiang Li; Zengbin Lu; Lili Li; Yi Yu; Song Dong; Xingyuan Men; Baohua Ye

doi:10.1371/journal.pone.0204097

Abstract

The bird cherry-oat aphid, Rhopalosiphum padi (L.), is a major insect pest of cereal crops in many countries. Imidacloprid has been widely used for controlling piercing-sucking insect pests worldwide, but its sublethal effects on R. padi have not been well addressed. In this study, we investigated the sublethal effects of imidacloprid on biological parameters and five enzyme activities of R. padi. The LC₁₀, LC₂₀, and LC₂₅ of imidacloprid to adult aphids were 0.0053, 0.0329 and 0.0659 mg L^-1, respectively. These concentrations significantly decreased pre-adult survival rate, but prolonged the development duration of 1^st instar nymphs, pre-oviposition period, and adult longevity. Adult oviposition period was also extended by LC₂₀. The intrinsic rate of increase (r), net reproductive rate (R₀), and finite rate (λ) decreased at all three concentrations, whereas mean generation time (T) increased. Moreover, LC₂₀ and LC₂₅ significantly inhibited superoxide dismutase (SOD) activity, but increased catalase (CAT) activity. Acetylcholinesterase (AChE) activity also increased at LC₂₀. However, cytochrome P450 enzyme and peroxidase (POD) activity did not differ between imidacloprid treatments and the control. In conclusion, the imidacloprid concentrations tested here have negative impacts on the performance of R. padi by reducing its nymphal survival, extending the development duration of some stages, decreasing the rate of population growth, and altering enzyme activities.

Citation: Li W, Lu Z, Li L, Yu Y, Dong S, Men X, et al. (2018) Sublethal effects of imidacloprid on the performance of the bird cherry-oat aphid Rhopalosiphum padi. PLoS ONE 13(9): e0204097. https://doi.org/10.1371/journal.pone.0204097

Editor: Nicolas Desneux, Institut Sophia Agrobiotech, FRANCE

Received: July 16, 2017; Accepted: September 3, 2018; Published: September 20, 2018

Copyright: © 2018 Li et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: All relevant data are within the paper and its Supporting Information files.

Funding: This work was supported by National Key R&D Program of China (2017YFD0200400) (XM), Natural Science Foundation of Shandong Province (ZR2016CB21) (ZL), Postdoctoral Innovation Project Special Funds of Shandong Province, and Agricultural Science and Technology Innovation Project of Shandong Academy of Agricultural Sciences (CXGC2016A09) (XM).

Competing interests: The authors have declared that no competing interests exist.

Introduction

Neonicotinoid insecticides, developed during the 1980s, have been widely applied to control piercing-sucking insect pests in various agricultural crops, with application to seeds, soil, and foliage [1–3]. They act as selective agonists of nicotinic acetylcholine receptors (nAChRs) in the central nervous system of insects, causing nervous stimulation at low to moderate concentrations, but leading to paralysis and death at high concentrations [4]. Many insect pests are effectively controlled by these insecticides [2, 3]. As systemic insecticides, they can travel through plant tissues and protect all parts of the crop [2]. However, because of their imbalanced distribution and degradation in the field [3,5,6], neonicotinoid insecticides, similar to other classes of insecticide, can not only cause direct mortality, but also result in sublethal effects on the exposed insects.

Sublethal effects have been described as effects on the physiology and behavior of an individual that has been exposed to an insecticide or toxin (the dose and/or concentration can be sublethal or lethal) [7]. Numerous studies have addressed this issue and showed that insecticides, including neonicotinoids, can cause sublethal effects on behavioral and physiological traits in arthropods, such as feeding activity, development duration, reproduction, host finding, and others [8–15]. For example, lower lethal concentrations of imidacloprid (LC₁₀ and LC₃₀) significantly affected the duration of phloem ingestion and decreased the developmental period of nymphs, adult longevity, and total fecundity of Aphis gossypii [9]. Additionally, few studies have investigated the sublethal effects of insecticides on enzymatic processes in insects [16–19]. Xiao et al. reported that acetylcholinesterase (AchE) activity decreased in both Rhopalosiphum padi and Sitobion avenae treated by LC₂₅ of pirimicarb [17]. Therefore, identifying and characterizing such sublethal effects is crucial to fully understand the relationships between the exposure dose of insecticides and insect response at both the individual and population levels.

Life tables are useful tools to assess the sublethal effects of insecticides on insects at the population level [20]. The age-stage, two-sex life table approach can provide more accurate estimates of population parameters, given that this approach considers both sexes and the variable developmental rate among individuals and can properly describe the development, stage differentiation, survival, and reproduction of the population [21–23]. It has been widely used to examine the responses of various herbivore species to doses and/or concentrations of insecticides [14, 23–26]. For example, when M. persicae adults were exposed to LC₃₀ of imidacloprid, the mean generation time (T) and gross reproductive rate (GRR) were significantly increased, whereas the intrinsic rate of increase (r) and finite rate of increase (λ) were reduced [24]. Thus, this method can provide a comprehensive assessment of sublethal effects of insecticides on arthropods at the population level.

The bird cherry-oat aphid, Rhopalosiphum padi (Hemiptera: Aphididae), a destructive pest of cereal crops worldwide, can cause direct damage by feeding on cereal plants and indirect damage by acting as vectors for the transmission of many viruses, including barley yellow dwarf virus (BYDV) [3, 27–30]. Outbreaks of this species have led to high yield losses of wheat in China [3]. Imidacloprid, the first commercially available neonicotinoid insecticide, has been applied extensively to control R. padi population in wheat fields [31]. However, its sublethal effects on R. padi have not yet been fully addressed. In this study, we investigated the sublethal effects of imidacloprid on the survival, development, fecundity, demographical parameters, and five enzyme activities of R. padi. This study aimed to determine the sublethal effects of imidacloprid on population and individual enzyme activity of R. padi; our results provide relevant information for the optimal use of imidacloprid against this pest.

Materials and methods

Ethics statement

No specific permits were required for the described experiments. The R. padi used in this study were originally collected from winter wheat fields at the Jinan Experimental Station of Shandong Academy of Agricultural Sciences (36.98°N, 116.98°E) and owned by the author’s institute (Institute of Plant Protection, Shandong Academy of Agricultural Sciences). None of the experiments involved any endangered or protected species.

Insects

The R. padi adults were initially collected from winter wheat fields at the Jinan Experimental Station of Shandong Academy of Agricultural Sciences (36.98° N, 116.98° E), Shandong Province, China, in 2014 and then maintained in climatic chambers at 23±1 ^oC, 60±10% relative humidity (RH) and a 16: 8 light: dark (L: D) photoperiod. These aphids were reared on insecticide-free wheat seedlings, which were changed weekly.

Insecticide and enzyme kits

Imidacloprid (CAS number: 138261-41-3, 95% purity) was purchased from Shandong Sino-agri United Biotechnology Co., Ltd (Jinan, Shandong Province, China). Kits for superoxide dismutase (SOD), peroxidase (POD), catalase (CAT), acetylcholinesterase (AChE), and cytochrome P450 enzyme were purchased from Suzhou Comin Biotechnology Co., Ltd (Suzhou, Jiangsu Province, China).

Acute toxicity of imidacloprid on R. padi

The acute toxicity of imidacloprid against R. padi adults was evaluated using the leaf-dip method [5, 32]. The stock solution of imidacloprid was prepared using analytical grade acetone, and then diluted with distilled water containing 0.5% Triton X-100 into five different concentrations: 10, 2, 0.4, 0.08 and 0.016 mg L^–1. Leaves were cut from insecticide-free wheat plants, dipped into insecticide solutions for 30 s, and placed in the shade to air dry for 2 h. These leaves were then placed with their abaxial surface downward in a Petri dish (9.0 cm in diameter) containing 2% agar to maintain humidity. Each treatment comprised three replicates of 30 adult aphids and there were five leaves used for each replication. Distilled water containing 0.5% Triton X-100 was used as the control. The Petri dishes were placed in climatic chambers at 23±1 ^oC, 60±10% RH, and a 16: 8 L: D photoperiod. Aphid mortalities were examined under a stereomicroscope at 24 h after exposure to imidacloprid. If the aphids were exposed to imidacloprid for longer than 24 h, the LC₅₀ value obtained would be lower than that at 24h.

Sublethal effects of imidacloprid on R. padi

LC₁₀ (0.0053 mg L^–1), LC₂₀ (0.0329 mg L^–1), and LC₂₅ (0.0659 mg L^–1) of imidacloprid were used in the life table experiment and distilled water containing 0.5% Triton X-100 was used as the control. The insecticide solutions were prepared as described in the ‘Acute toxicity of imidacloprid on R. padi’ section. The cut leaves were dipped into each imidacloprid solution and control solution for 30 s, placed in the shade to air dry for 2 h, and then put with their abaxial surface downward in a Petri dish (9.0 cm in diameter) containing 2% agar to maintain humidity. Adult aphids without exposure to any insecticide were allowed to feed on the treated leaves for 24 h. After that, the surviving adult aphids were individually transferred to new, smaller Petri dishes (3.5 cm in diameter) containing 2% agar with insecticide-free leaves. After 24 h, the adults were removed and only one nymph was left in each Petri dish. Each treatment contained 30 neonate nymphs. The survival rate, development duration, and the number of nymphs produced per aphid were recorded daily under a stereomicroscope until the death of the adult. The wheat leaves were changed every 5 days. All the experiments were conducted in climatic chambers at 23±1 ^oC, 60±10% RH, and a 16: 8 L: D photoperiod.

Enzyme activity determination

Adult aphids were allowed to feed on wheat leaves treated with LC₁₀, LC₂₀, or LC₂₅ of imidacloprid and distilled water containing 0.5% Triton X-100 for 24 h. Each treatment was repeated three times. Any surviving adult aphids were collected for each replication, immediately frozen in liquid nitrogen, and stored at –80°C until use.

Enzyme preparation: approximately 0.1 g frozen aphids was homogenized in 1 mL ice-cold phosphate buffer (0.1 M, pH 7.5, containing 0.5% Triton X-100) and centrifuged at 8000 g (Eppendorf centrifuge 5417R, Germany), 4 ^oC for 10 min. The supernatants were then used for the enzyme activity assays for SOD, POD, AChE, and P450. For CAT, approximately 0.2 g frozen aphids was homogenized in 0.2 mL normal saline and centrifuged at 8000 g, 4°C for 10 min. The supernatants were then used for the CAT activity assay. All optical densities (OD) were measured at different optimum wavelengths using an Emax Plus Molecular Device (Molecular Devices, Sunnyvale, California, USA).

SOD activity: the mixture contained 18 μL enzyme preparation, 45 μL EDTA, 100 μL xanthine, and 2 μL xanthine oxidase. The reaction was stopped by the addition of 36 μL NBT after incubation at 27 ^oC for 30 min. The control samples contained no enzyme during the incubation. The OD was measured at 560 nm.

POD activity: the mixture contained 15 μL enzyme preparation, 270 μL distilled water, 520 μL sodium acetate and acetic acid solution, 30 μL hydrogen peroxide and 135 μL guaiacol solution. The reaction was stopped by the addition of 36 μL of NBT after incubation at 27 ^oC for 30 min. The OD was measured at 30 s and 90 s at 470 nm.

CAT activity: the mixture contained 0.05 mL enzyme preparation, 0.1 mL hydrogen peroxide, and 0.01 mL phosphate buffer, and was incubated at 37°C for 1 min. Then, 0.1 mL reagent C and 0.01 mL reagent D were added to the mixture. The OD was measured at 240 nm.

AChE activity: all the reagents were added to Eppendorf tubes according to protocols of the AChE activity kit provided by Suzhou Comin Biotechnology Co., Ltd. The OD was measured at 412 nm.

P450 activity: the mixtures containing either 50 μL standard or sample and 50 μL enzyme conjugate was incubated at 37°C for 30 min. Then, 50 μL substrate A and 50 μL substrate B were added. Each test tube was again incubated at 37°C for 10 min in the dark. The reaction was stopped by adding 50 μL of the stop solution. The OD was measured at 450 nm within 15 min of the reaction being stopped.

Data analysis

The mortality data for each imidacloprid treatment were corrected relative to the control group. LC₁₀, LC₂₀, LC_25, and LC₅₀ were calculated by probit analysis in SPSS v18.0 software (IBM Inc., New York, USA). Data on enzyme activities were analyzed by one-way ANOVA followed by Tukey’s multiple-range test. The raw data of development and reproduction of individual insects (survival, longevity, and female daily fecundity) were analyzed using TWOSEX-MSChart [33] computer program according to the theory for the age-stage, two-sex life table [21–23]. The age- stage-specific survival rate (s_xj, x is age and j is the stage), the age-specific survival rate (l_x), the age-stage-specific fecundity (f_xj), and the age-specific fecundity (m_x) were calculated. Four demographic parameters were further obtained based on the l_x and m_x. The net reproductive rate (R₀) was calculated using Eq 1:

The intrinsic rate of increase (r) was estimated using the iterative bisection method (Eq 2):

The finite rate (λ) was calculated using Eq 3:

The mean generation time (T) was calculated using Eq 4:

The means and standard errors of life table parameters were estimated using a bootstrap procedure with a bootstrap number m = 100, 000 to ensure more precise estimates [34]. The paired bootstrap test was used to compare the differences in survival rate, development time, longevity, fecundity, and life table parameters among the treatments based on the confidence interval of differences [26, 35–37]. SigmaPlot 12.0 software (Systat Software Inc., San Jose, CA) was used to create the figures.

Results

Acute toxicity of imidacloprid on R. padi

The regression equation obtained from the concentration-mortality response bioassay at 24 h was: Y = 0.5609 X + 4.9654 (χ² = 2.75, P = 0.432, r = 0.88, where X represents the log-transform of concentrations of imidacloprid and Y represents the probability value of aphid mortalities). The LC₁₀, LC₂₀, LC₂₅, and LC₅₀ of imidacloprid against R. padi adults were 0.0053 (95% confidence interval: 0.0003–0.0979 mg L^–1), 0.0329 (0.0046–0.2373 mg L^–1), 0.0659 (0.0125–0.3463 mg L^–1) and 1.084 mg L^-1 (0.3222–3.6471 mg L^–1), respectively.

Sublethal effects of imidacloprid on biological parameters of R. padi

The survival, development, fecundity, and life table parameters are presented in Table 1. The developmental duration of 1^st instar nymphs (N1) and pre-oviposition period of adults at LC₁₀, LC₂₀, and LC₂₅ were significantly longer than those of the control. By contrast, the survival rate of pre-adult aphids was significantly lower at all these concentrations. Adult longevity was significantly lengthened by LC₂₀ and LC₂₅, and aphids exposed to LC₂₀ also had a longer oviposition period. However, the developmental duration of 2^nd instar nymphs (N2) and the duration from 3^rd to 4^th instar nymphs (N3-N4) did not differ between each imidacloprid concentration and the control. The number of nymphs laid by each female adult was also not different between imidacloprid treatment and control.

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Table 1. Effects of three concentrations of imidacloprid on biological and demographic parameters of Rhopalosiphum padi.

https://doi.org/10.1371/journal.pone.0204097.t001

The intrinsic rate of increase (r) and finite rate of increase (λ) of aphids from all exposed concentrations were significantly lower than those of the control. The aphids exposed to LC₁₀ and LC₂₅ also had a lower net reproductive rate (R₀). However, the mean generation time (T) significantly increased at all the three concentrations.

The age-stage-specific survival rate (s_xj) depicts the probability that a newborn will survive to age x and stage j (Fig 1). Given the variability in interindividual development rates, there was overlap between stages for each concentration treatment and control.

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Fig 1. Age-stage-specific survival rates (s_xj) of Rhopalosiphum padi, the parental females of which were exposed to wheat leaves treated with different concentrations of imidacloprid.

(a) Control, (b) LC₁₀, (c) LC₂₀, (d) LC₂₅.

https://doi.org/10.1371/journal.pone.0204097.g001

The age-specific survival rate (l_x), age-specific fecundity (m_x), and net maternity (l_xm_x) are shown in Fig 2. The survival rate of aphids decreased with age and the maximal survival time was 38, 36, 37, and 28 d for LC₁₀, LC₂₀, LC₂₅, and control, respectively. In the curve m_x, the peak fecundity occurred in the LC₁₀, LC₂₀, LC₂₅, and control at the age of 17, 10, 11, and 12 d, respectively. The highest fecundity was 3.45, 4.47, 4.25, and 4.42 offspring, respectively. The maximal l_xm_x values appeared at the age of 11, 10, 11, and 11 d, with a mean number of 1.67, 2.53, 1.70, and 3.53 offspring for the LC₁₀, LC₂₀, LC₂₅, and control, respectively.

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Fig 2. Age-specific survival rates (l_x), age-specific fecundity (m_x) and net maternity (l_xm_x) of Rhopalosiphum padi, the parental females of which were exposed to wheat leaves treated with different concentrations of imidacloprid.

(a) Control, (b) LC₁₀, (c) LC₂₀, (d) LC₂₅.

https://doi.org/10.1371/journal.pone.0204097.g002

The age-stage-specific reproductive values (v_xj, which denotes the expectation of future offspring for individuals of R. padi at age x and stage j) are shown in Fig 3. With the extension of age and stage, v_xj gradually increased at first and then decreased in the three treatments and control. The highest v_xj values occurred in the LC₁₀, LC₂₀, LC₂₅, and control at the age of 10, 10, 9, and 8 d, respectively. The highest v_xj values were 13.90, 16.66, 15.91, and 12.93 offspring, respectively.

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Fig 3. Age-stage-specific reproductive value (v_xj) of Rhopalosiphum padi, the parental females of which were exposed to wheat leaves treated with different concentrations of imidacloprid.

(a) Control, (b) LC₁₀, (c) LC₂₀, (d) LC₂₅.

https://doi.org/10.1371/journal.pone.0204097.g003

Sublethal effects of imidacloprid on enzyme activity of R. padi

The five enzyme activities are shown in Table 2. LC₂₀ and LC₂₅ significantly inhibited the SOD activity of aphids, but increased CAT activity. AChE activity increased significantly at LC₂₀. However, P450 and POD activities were not significantly different between the three imidacloprid treatments and control.

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Table 2. Effects of three concentrations of imidacloprid on five enzyme activities of Rhopalosiphum padi.

https://doi.org/10.1371/journal.pone.0204097.t002

Discussion

Our results showed that exposure to three concentrations of imidacloprid resulted in the duration of 1^st instar nymphs (N1), pre-oviposition period, and adult longevity of R. padi being significantly longer than those of the control (Table 1). These findings have been reported by previous studies on Aphis glycines [38], Myzus persicae [24], R. padi [10], and A. gossypii [39]. Zeng et al. reported that the nymphal period, pre-oviposition period, and female longevity of M. persicae were significantly prolonged when adults were exposed to LC₃₀ (0.541 mg L^–1) of imidacloprid [24]. By contrast, reduced nymphal development duration and adult longevity were observed on A. gossypii [9, 11] and Apolygus lucorum [15] exposed to sublethal concentrations of neonicotinoids. Koo et al. showed that the development period of A. gossypii nymphs was shorter at LC₃₀ (0.82 mg L^–1) of imidacloprid [9]. The differences in development rate of insect pests exposed to plants treated with neonicotinoid might be caused by changes in their feeding behavior. Low concentrations of imidacloprid have antifeedant effects, as determined by honeydew excretion and feeding behavior studies [9, 12, 24, 31, 39, 40]. This property can negatively affect nutrition absorption, disrupt the hormone balance, and might induce a trade-off between development and fecundity.

We also found that aphids exposed to LC₁₀ and LC₂₅ had a lower net reproductive rate (R₀). This could be attributed to the higher mortality in nymphal stages of R. padi at these two concentrations with a mortality of 50% and 60%, respectively, compared with 17% in control (Table 1 and Fig 2). Zeng et al. reported that the pre-adult survivorship of M. persicae exposed to LC₃₀ of imidacloprid was lower (70%) than that of the control (91.67%) [24]. Moreover, there was no significant difference between each imidacloprid concentration and the control in terms of the fecundity of female adult aphids. Miao et al. showed that the fertility of Sitobion avenae feeding on wheat plants treated with LC₁₀ of imidacloprid, dinotefuran, thiacloprid, and thiamethoxam was not affected [31]. Lu et al. demonstrated that 3 h exposure to sublethal doses of imidacloprid for one generation had no discernible effect on the fecundity of either S. avenae or R. padi [18]. However, numerous studies reported that lower concentrations of imidacloprid can induce higher fecundity of exposed insects, such as A. glycines [38], M. persicae [5, 19, 24], and A. gossypii [11]. Qu et al. reported that 0.05 mg L^–1 imidacloprid significantly increased the cumulative offspring per aphid, whereas this was significantly reduced by 0.2 mg L^–1 [38]. This phenomenon might be related to hormesis, which is the stimulation of organism performance at low levels of exposure to a toxic agent that is normally toxic at high levels of exposure [41]. Hormesis is often implicated as the primary mechanism for the resurgence of pest populations [42, 43]. Additionally, the intrinsic rate of increase (r) and finite rate of increase (λ) of aphids from all exposed concentrations were significantly lower than those of the control (Table 1), which might indicate that the concentrations of imidacloprid tested here can suppress the population growth of R. padi. Given that fecundity did not differ between the imidacloprid treatment and control, the lower survival rate of nymphal stages in aphids from imidacloprid treatment could lead to such a difference. Zeng et al. reported that M. persicae treated with LC₃₀ imidacloprid also showed lower r and λ [24]. In addition, 0.20 mg L^-1 imidacloprid significantly reduced r and λ of A. glycines population and might suppress their population growth through a reduction in survival and reproduction activity [38]. Therefore, these three concentrations of imidacloprid could negatively impact the performance of R. padi at the population level by changing key biological parameters.

Sublethal exposure might also lead to changes in the physiological traits of insects [7]. Several studies have reported that sublethal concentrations and/or doses of insecticides altered the enzyme activities, detoxification gene expression, and carboxylesterase expression of exposed insects, such as R. padi [18], S. avenae [18], M. persicae [19], Porcellio scaber [44], Megacopta cribraria [45], Chironomus riparius [46], and A. gossypii [47]. Lu et al. showed that 3 h exposure to a sublethal dose of imidacloprid for one generation induced the activity of carboxylesterase (CarE) but inhibited the activity of glutathione S-transferase (GST) in S. avenae and R. padi [18]. Rix et al. showed that 0.25 and 2.5 μg L^–1 imidacloprid significantly increased or decreased the expression of genes encoding E4-esterase and cytochrome P450-CYP6CY3 in M. persicae, with variation within and across generations [19]. In the current study, we found that lower concentrations of imidacloprid (LC₂₀ or LC₂₅) inhibited the SOD activity of R. padi, but increased the activities of CAT and AChE. Given that SOD activity was inhibited by imidacloprid, harmful superoxide free radicals could not be fully catalyzed into hydrogen peroxide (H₂O₂) and might accumulate in the body of R. padi. The increased CAT activity could help these aphids degrade some of this H₂O₂ and protect them from oxidative damage. Moreover, although AChE is not a molecular target of imidacloprid and has no role in the detoxification of insecticides, it is an important biochemical marker in ecotoxicology. The increased AChE activity of R. padi treated with LC₂₀ indicates that an excess of acetylcholine might exist in the synaptic cleft and promote a higher activity of AChE. Another study also showed that LC₄₀ of imidacloprid increased AChE activity in M. cribraria [45]. Similarly, P450 has an important role in the detoxification of xenobiotics, including pesticides, and its mediated detoxification is one of the major mechanisms of insecticide resistance [48–50]. In our experiment, the absence of effects on P450 activity demonstrates that the imidacloprid concentrations used in the life table experiment might not reach the threshold that induces the response of adult aphids. Thus, R. padi alters its enzyme activities to counter the negative effects resulting from imidacloprid.

In conclusion, our laboratory study showed that the concentrations of imidacloprid investigated negatively affected the performance of R. padi by reducing its nymphal survival, extending the development duration of some stages, suppressing population growth, and altering enzyme activities. The most important finding was that imidacloprid, even at a lower concentration (LC₁₀: 0.0053 mg L^–1), significantly reduced the survival rate of pre-adult aphids and suppressed their population growth rate. This would be helpful in controlling populations of this aphid in the field, because lower concentrations of this insecticide can effectively reduce the insect population size, reducing the ecological risks to biodiversity and beneficial insects, especially natural enemies. However, because of the complexity of field conditions, more trials should be carried out in the field to fully assess the suitability and safety of these concentrations selected in laboratory study.

Supporting information

S1 Table. Spread sheet tables presenting supplementary data.

https://doi.org/10.1371/journal.pone.0204097.s001

(XLSX)

Acknowledgments

We are very grateful to the students from Jinan University for conducting the life table study experiment. This work was supported by National Key R&D Program of China (2017YFD0200400), Natural Science Foundation of Shandong Province (ZR2016CB21), Postdoctoral Innovation Project Special Funds of Shandong Province, and Agricultural Science and Technology Innovation Project of Shandong Academy of Agricultural Sciences (CXGC2016A09).

References

1. Kollmeyer WD, Flattum RF, Foster JP, Powell JE, Schroeder ME, Soloway SB. Discovery of the nitromethylene heterocycle insecticides. In: Yamamoto I, Casida JE, editors. Nicotinoid Insecticides and the Nicotinic Acetylcholine Receptor. Tokyo: Springer-Verlag; 1999. pp. 71–89.
2. Goulson D. An overview of the environmental risks posed by neonicotinoid insecticides. J Appl Ecol. 2013; 50: 997–987.
- View Article
- Google Scholar
3. Zhang P, Zhang XF, Zhao YH, Wei Y, Mu W, Liu F. Effects of imidacloprid and clothianidin seed treatments on wheat aphids and their natural enemies on winter wheat. Pest Manag Sci. 2016; 72: 1141–1149. pmid:26248607
- View Article
- PubMed/NCBI
- Google Scholar
4. Tomizawa M, Casida JE. Neonicotinoid insecticide toxicology: mechanisms of selective action. Annu Rev Pharmacol Toxicol. 2005; 45: 247–268. pmid:15822177
- View Article
- PubMed/NCBI
- Google Scholar
5. Cutler GC, Ramanaidu K, Astatkie T, Ismana MB. Green peach aphid, Myzus persicae (Hemiptera: Aphididae), reproduction during exposure to sublethal concentrations of imidacloprid and azadirachtin. Pest Manag Sci. 2009; 65: 205–209. pmid:19089851
- View Article
- PubMed/NCBI
- Google Scholar
6. Biondi A, Desneux N, Siscaro G, Zappalà L. Using organic-certified rather than synthetic pesticides may not be safer for biological control agents: selectivity and side effects of 14 pesticides on the predator Orius laevigatus. Chemosphere. 2012; 87: 803–812. pmid:22342338
- View Article
- PubMed/NCBI
- Google Scholar
7. Desneux N, Decourtye A, Delpuech JM. The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol. 2007; 52: 81–106. pmid:16842032
- View Article
- PubMed/NCBI
- Google Scholar
8. Haynes KF. Sublethal effects of neurotoxic insecticides on insect behavior. Annu Rev Entomol. 1988; 33: 149–168. pmid:3277528
- View Article
- PubMed/NCBI
- Google Scholar
9. Koo HN, Lee SW, Yun SH, Kim HK, Kim GH. Feeding response of the cotton aphid, Aphis gossypii, to sublethal rates of flonicamid and imidacloprid. Entomol Exp Appl. 2015; 154: 110–119.
- View Article
- Google Scholar
10. Daniels M, Bale JS, Newbury HJ, Lind RJ, Pritchard J. A sublethal dose of thiamethoxam causes a reduction in xylem feeding by the bird cherry-oat aphid (Rhopalosiphum padi), which is associated with dehydration and reduced performance. J Insect Physiol. 2009; 55: 758–765. pmid:19482292
- View Article
- PubMed/NCBI
- Google Scholar
11. Wang SY, Qi YF, Desneux N, Shi XY, Biondi A, Gao XW. Sublethal and transgenerational effects of short-term and chronic exposures to the neonicotinoid nitenpyram on the cotton aphid Aphis gossypii. J Pest Sci. 2016; 90: 389–396.
- View Article
- Google Scholar
12. He YX, Zhao JW, Zheng Y, Weng QY, Biondi A, Desneuc N, et al. Assessment of potential sublethal effects of various insecticides on key biological traits of the tobacco whitefly, Bemisia tabaci. Int J Bio Sci. 2013; 9: 246–255.
- View Article
- Google Scholar
13. Tappert L, Pokorny T, Hofferberth J, Ruther J. Sublethal doses of imidacloprid disrupt sexual communication and host finding in a parasitoid wasp. Sci Rep. 2017; 7: 42756. pmid:28198464
- View Article
- PubMed/NCBI
- Google Scholar
14. Qu YY, Xiao D, Liu JJ, Chen Z, Song LF, Desneux N, et al. Sublethal and hormesis effects of beta-cypermethrin on the biology, life table parameters and reproductive potential of soybean aphid Aphis glycines. Ecotoxicology. 2017; 26: 1002–1009. pmid:28685415
- View Article
- PubMed/NCBI
- Google Scholar
15. Tan Y, Biondi A, Desneux N, Gao XW. Assessment of physiological sublethal effects of imidacloprid on the mirid bug Apolygus lucorum (Meyer-dür). Ecotoxicology. 2012; 21: 1989–1997. pmid:22740097
- View Article
- PubMed/NCBI
- Google Scholar
16. Rumpf S, Hetzel F, Frampton C. Lacewings (Neuroptera: Hemerobiidae and Chrysopidae) and integrated pest management: enzyme activity as biomaker of sublethal insecticide exposure. J Econ Entomol. 1997; 90: 102–108.
- View Article
- Google Scholar
17. Xiao D, Yang T, Desneux N, Han P, Gao XW. Assessment of sublethal and transgenerational effects of pirimicarb on the wheat aphids Rhopalosiphum padi and Sitobion avenae. PLoS ONE. 2015; 10: e0128936. pmid:26121265
- View Article
- PubMed/NCBI
- Google Scholar
18. Lu YH, Zheng XS, Gao XW. Sublethal effects of imidacloprid on the fecundity, longevity, and enzymes activity of Sitobion avenae (Fabrcius) and Rhopalosiphum padi (Linnaeus). Bull Entomol Res. 2016; 106: 551–559. pmid:27161277
- View Article
- PubMed/NCBI
- Google Scholar
19. Rix RR, Ayyanath MM, Cutler GC. Sublethal concentrations of imidacloprid increase reproduction, alter expression of detoxification genes, and prime Myzus persicae for subsequent stress. J Pest Sci. 2016; 89: 581–589.
- View Article
- Google Scholar
20. Stark JD, Banks JE. Population-level effects of pesticides and other toxicants on arthropods. Annu Rev Entomol. 2003; 48: 505–519. pmid:12221038
- View Article
- PubMed/NCBI
- Google Scholar
21. Chi H, Liu H. Two new methods for the study of insect population ecology. Bull Inst Zool Acad Sinica. 1985; 24: 225–240.
- View Article
- Google Scholar
22. Chi H. Life-table analysis incorporating both sexes and variable development rates among individuals. Environ Entomol. 1988; 17: 26–34.
- View Article
- Google Scholar
23. Chi H, Su HY. Age-stage, two-sex life tables of Aphidius gifuensis (Ashmead) (Hymenoptera: Braconidae) and its host Myzus persicae (Sulzer) (Homoptera: Aphididae) with mathematical proof of the relationship between female fecundity and the net reproductive rate. Environ Entomol. 2006; 35: 10–21.
- View Article
- Google Scholar
24. Zeng XY, He YQ, Wu JX, Tang YM, Gu J, Ding W, et al. Sublethal effects of cyantraniliprole and imidacloprid on feeding behavior and life table parameters of Myzus persicae (Hemiptera: Aphididae). J Econ Entomol. 2016; 109: 1595–1602. pmid:27247299
- View Article
- PubMed/NCBI
- Google Scholar
25. Chen XW, Ma KS, Li F, Liang PZ, Liu Y, Guo TF, et al. Sublethal and transgenerational effects of sulfoxaflor on the biological traits of the cotton aphid, Aphis gossypii Glover (Hemiptera: Aphididae). Ecotoxicology. 2016; 25: 1841–1848. pmid:27670668
- View Article
- PubMed/NCBI
- Google Scholar
26. Saska P, Skuhrovec J, Lukáš J, Chi H, Tuan SJ, Honěk A. Treatment by glyphosate-based herbicide alters life history parameters of the rose-grain aphid Metopolophium dirhodum. Sci Rep. 2016; 6: 27801. pmid:27302015
- View Article
- PubMed/NCBI
- Google Scholar
27. Chu JX. Agricultural Entomology. Beijing: China Agricultural Press; 2009.
28. Wang SB, Chen B, Wang Y, Bu HM. Synthesis discussion of prevention and cure on wheat aphid and yellow dwarf. J Shanxi Agric Sci. 2003; 31: 69–71.
- View Article
- Google Scholar
29. Gray SM, Bergstrom GC, Vaughan R, Simth DM, Kalb DW. Insecticidal control of cereal aphids and its impact on the epidemiology of the barley yellow dwarf luteoviruses. Crop Prot. 1996; 15: 687–697.
- View Article
- Google Scholar
30. Brault V, Herrbach É, Reinbold C. Electron microscopy studies on luteovirid transmission by aphids. Micron. 2007; 38: 302–312. pmid:16750376
- View Article
- PubMed/NCBI
- Google Scholar
31. Miao J, Du ZB, Wu YQ, Gong ZJ, Jiang YL, Duan Y, et al. Sub-lethal effects of four neonicotinoid seed treatments on the demography and feeding behaviour of the wheat aphid Sitobion avenae. Pest Manag Sci. 2014; 70: 55–59. pmid:23457039
- View Article
- PubMed/NCBI
- Google Scholar
32. Moores GD, Gao XW, Denholm I, Devonshire AL. Characterisation of insensitive acetylcholinesterase in insecticide resistant cotton aphids, Aphis gossypii Glover (Homoptera: Aphididae). Pestic Biochem Physiol. 1996; 56:102–110
- View Article
- Google Scholar
33. Chi H. TWOSEX-MSChart: a computer program for the age-stage, two-sex life table analysis. 2018; 2:20. Available from: http://140.120.197.173/Ecology/Download/TWOSEX-MSChart-B100000.rar
- View Article
- Google Scholar
34. Efron B, Tibshirani RJ. An Introduction to the Bootstrap. Boca Raton, London, New York, Washington, D.C.: Chapman and Hall/CRC; 1994.
35. Reddy GVP, Chi H. Demographic comparison of sweetpotato weevil reared on a major host, Ipomoea batatas, and an alternative host, I. triloba. Sci Rep, 2015; 5: 11871. pmid:26156566
- View Article
- PubMed/NCBI
- Google Scholar
36. Brandstätter E. Confidence intervals as an alternative to significance testing. Methods of Psychological Research Online. 1999; 4: 33–46. (Internet: http://www.ipn.uni-kiel.de/mpr/)
- View Article
- Google Scholar
37. Huang YB, Chi H. Assessing the application of the Jackknife and Bootstrap techniques to the estimation of the variability of the net reproductive rate and gross reproductive rate: a case study in Bactrocera cucurbitae (Coquillett) (Diptera: Tephritidae). J Agric & Fore. 2012; 61: 37–45.
- View Article
- Google Scholar
38. Qu YY, Xiao D, Li JY, Chen Z, Biondi A, Desneux N, et al. Sublethal and hormesis effects of imidacloprid on the soybean aphid Aphis glycines. Ecotoxicology. 2015; 24: 479–487. pmid:25492586
- View Article
- PubMed/NCBI
- Google Scholar
39. Gerami S, Jahromi KT, Ashouri A, Rasoulian G, Heidari A. Sublethal effects of imidacloprid and pymetrozine on the life table parameters of Aphis gossypii Glover (Homoptera: Aphididae). Comm Appl Biol Sci. 2005; 70:779–785.
- View Article
- Google Scholar
40. Nauen R, Koob B, Elbert A. Antifeedant effects of sublethal dosages of imidacloprid on Bemisia tabaci. Entomol Exp Appl. 1998; 88: 287–293.
- View Article
- Google Scholar
41. Calabrese EJ, Baldwin LA. Hormesis: a generalizable and unifying hypothesis. Crit Rev Toxicol. 2001; 31: 353–424. pmid:11504172
- View Article
- PubMed/NCBI
- Google Scholar
42. Cordeiro EM, de Moura IL, Fadini MA, Guedes RN. Beyond selectivity: are behavioural avoidance and hormesis likely causes of pyrethroid-induced outbreaks of the southern red mite Oligonychus ilicis? Chemosphere. 2013; 93: 1111–1116. pmid:23830118
- View Article
- PubMed/NCBI
- Google Scholar
43. Guedes RN, Cutler GC. Insecticide-induced hormesis and arthropod pest management. Pest Manag Sci. 2014; 70: 690–697. pmid:24155227
- View Article
- PubMed/NCBI
- Google Scholar
44. Drobne D, Blažič M, Van Gestel CA, Lešer V, Zidar P, Jemec A, et al. Toxicity of imidacloprid to the terrestrial isopod Porcellio scaber (Isopoda, Crustacea). Chemosphere. 2008; 71: 1326–1334. pmid:18190949
- View Article
- PubMed/NCBI
- Google Scholar
45. Miao J, Reisig DD, Li GP, Wu YQ. Sublethal effects of insecticide exposure on Megacopta cribraria (Fabricius) nymphs: key biological traits and acetylcholinesterase activity. J Insect Sci. 2016; 16: 99; 1–6.
- View Article
- Google Scholar
46. Azevedo-Pereira HMVS, Lemos MFL, Soares AMVM. Effects of imidacloprid exposure on Chironomus riparius Meigen larvae: linking acetylcholinesterase activity to behaviour. Ecotoxicol. Environ Saf. 2011; 74: 1210–1215. pmid:21511337
- View Article
- PubMed/NCBI
- Google Scholar
47. Gong YH, Shi XY, Desneux N, Gao XW. Effects of spirotetramat treatments on fecundity and carboxylesterase expression of Aphis gossypii Glover. Ecotoxicology. 2016; 25: 655–663. pmid:26898726
- View Article
- PubMed/NCBI
- Google Scholar
48. Wen YC, Liu ZW, Bao HB, Han ZJ. Imidacloprid resistance and its mechanisms in field populations of brown planthopper, Nilaparvata lugens Stål in China. Pestic Biochem Physiol. 2009; 94: 36–42.
- View Article
- Google Scholar
49. Zhang YX, Yang YX, Sun HH, Liu ZZ. Metabolic imidacloprid resistance in the brown planthopper, Nilaparvata lugens, relies on multiple P450 enzymes. Insect Biochem Mol Biol. 2016; 79: 50–56. pmid:27793627
- View Article
- PubMed/NCBI
- Google Scholar
50. Puinean AM, Foster SP, Oliphant L, Denholm I, Field LM, Millar NS, et al. Amplification of a cytochrome P450 gene is associated with resistance to neonicotinoid insecticides in the aphid Myzus persicae. PLoS Genet. 2010; 6: e1000999. pmid:20585623
- View Article
- PubMed/NCBI
- Google Scholar

[ref1] 1. Kollmeyer WD, Flattum RF, Foster JP, Powell JE, Schroeder ME, Soloway SB. Discovery of the nitromethylene heterocycle insecticides. In: Yamamoto I, Casida JE, editors. Nicotinoid Insecticides and the Nicotinic Acetylcholine Receptor. Tokyo: Springer-Verlag; 1999. pp. 71–89.

[ref2] 2. Goulson D. An overview of the environmental risks posed by neonicotinoid insecticides. J Appl Ecol. 2013; 50: 997–987.
View Article
Google Scholar

[3] View Article

[4] Google Scholar

[ref3] 3. Zhang P, Zhang XF, Zhao YH, Wei Y, Mu W, Liu F. Effects of imidacloprid and clothianidin seed treatments on wheat aphids and their natural enemies on winter wheat. Pest Manag Sci. 2016; 72: 1141–1149. pmid:26248607
View Article
PubMed/NCBI
Google Scholar

[6] View Article

[7] PubMed/NCBI

[8] Google Scholar

[ref4] 4. Tomizawa M, Casida JE. Neonicotinoid insecticide toxicology: mechanisms of selective action. Annu Rev Pharmacol Toxicol. 2005; 45: 247–268. pmid:15822177
View Article
PubMed/NCBI
Google Scholar

[10] View Article

[11] PubMed/NCBI

[12] Google Scholar

[ref5] 5. Cutler GC, Ramanaidu K, Astatkie T, Ismana MB. Green peach aphid, Myzus persicae (Hemiptera: Aphididae), reproduction during exposure to sublethal concentrations of imidacloprid and azadirachtin. Pest Manag Sci. 2009; 65: 205–209. pmid:19089851
View Article
PubMed/NCBI
Google Scholar

[14] View Article

[15] PubMed/NCBI

[16] Google Scholar

[ref6] 6. Biondi A, Desneux N, Siscaro G, Zappalà L. Using organic-certified rather than synthetic pesticides may not be safer for biological control agents: selectivity and side effects of 14 pesticides on the predator Orius laevigatus. Chemosphere. 2012; 87: 803–812. pmid:22342338
View Article
PubMed/NCBI
Google Scholar

[18] View Article

[19] PubMed/NCBI

[20] Google Scholar

[ref7] 7. Desneux N, Decourtye A, Delpuech JM. The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol. 2007; 52: 81–106. pmid:16842032
View Article
PubMed/NCBI
Google Scholar

[22] View Article

[23] PubMed/NCBI

[24] Google Scholar

[ref8] 8. Haynes KF. Sublethal effects of neurotoxic insecticides on insect behavior. Annu Rev Entomol. 1988; 33: 149–168. pmid:3277528
View Article
PubMed/NCBI
Google Scholar

[26] View Article

[27] PubMed/NCBI

[28] Google Scholar

[ref9] 9. Koo HN, Lee SW, Yun SH, Kim HK, Kim GH. Feeding response of the cotton aphid, Aphis gossypii, to sublethal rates of flonicamid and imidacloprid. Entomol Exp Appl. 2015; 154: 110–119.
View Article
Google Scholar

[30] View Article

[31] Google Scholar

[ref10] 10. Daniels M, Bale JS, Newbury HJ, Lind RJ, Pritchard J. A sublethal dose of thiamethoxam causes a reduction in xylem feeding by the bird cherry-oat aphid (Rhopalosiphum padi), which is associated with dehydration and reduced performance. J Insect Physiol. 2009; 55: 758–765. pmid:19482292
View Article
PubMed/NCBI
Google Scholar

[33] View Article

[34] PubMed/NCBI

[35] Google Scholar

[ref11] 11. Wang SY, Qi YF, Desneux N, Shi XY, Biondi A, Gao XW. Sublethal and transgenerational effects of short-term and chronic exposures to the neonicotinoid nitenpyram on the cotton aphid Aphis gossypii. J Pest Sci. 2016; 90: 389–396.
View Article
Google Scholar

[37] View Article

[38] Google Scholar

[ref12] 12. He YX, Zhao JW, Zheng Y, Weng QY, Biondi A, Desneuc N, et al. Assessment of potential sublethal effects of various insecticides on key biological traits of the tobacco whitefly, Bemisia tabaci. Int J Bio Sci. 2013; 9: 246–255.
View Article
Google Scholar

[40] View Article

[41] Google Scholar

[ref13] 13. Tappert L, Pokorny T, Hofferberth J, Ruther J. Sublethal doses of imidacloprid disrupt sexual communication and host finding in a parasitoid wasp. Sci Rep. 2017; 7: 42756. pmid:28198464
View Article
PubMed/NCBI
Google Scholar

[43] View Article

[44] PubMed/NCBI

[45] Google Scholar

[ref14] 14. Qu YY, Xiao D, Liu JJ, Chen Z, Song LF, Desneux N, et al. Sublethal and hormesis effects of beta-cypermethrin on the biology, life table parameters and reproductive potential of soybean aphid Aphis glycines. Ecotoxicology. 2017; 26: 1002–1009. pmid:28685415
View Article
PubMed/NCBI
Google Scholar

[47] View Article

[48] PubMed/NCBI

[49] Google Scholar

[ref15] 15. Tan Y, Biondi A, Desneux N, Gao XW. Assessment of physiological sublethal effects of imidacloprid on the mirid bug Apolygus lucorum (Meyer-dür). Ecotoxicology. 2012; 21: 1989–1997. pmid:22740097
View Article
PubMed/NCBI
Google Scholar

[51] View Article

[52] PubMed/NCBI

[53] Google Scholar

[ref16] 16. Rumpf S, Hetzel F, Frampton C. Lacewings (Neuroptera: Hemerobiidae and Chrysopidae) and integrated pest management: enzyme activity as biomaker of sublethal insecticide exposure. J Econ Entomol. 1997; 90: 102–108.
View Article
Google Scholar

[55] View Article

[56] Google Scholar

[ref17] 17. Xiao D, Yang T, Desneux N, Han P, Gao XW. Assessment of sublethal and transgenerational effects of pirimicarb on the wheat aphids Rhopalosiphum padi and Sitobion avenae. PLoS ONE. 2015; 10: e0128936. pmid:26121265
View Article
PubMed/NCBI
Google Scholar

[58] View Article

[59] PubMed/NCBI

[60] Google Scholar

[ref18] 18. Lu YH, Zheng XS, Gao XW. Sublethal effects of imidacloprid on the fecundity, longevity, and enzymes activity of Sitobion avenae (Fabrcius) and Rhopalosiphum padi (Linnaeus). Bull Entomol Res. 2016; 106: 551–559. pmid:27161277
View Article
PubMed/NCBI
Google Scholar

[62] View Article

[63] PubMed/NCBI

[64] Google Scholar

[ref19] 19. Rix RR, Ayyanath MM, Cutler GC. Sublethal concentrations of imidacloprid increase reproduction, alter expression of detoxification genes, and prime Myzus persicae for subsequent stress. J Pest Sci. 2016; 89: 581–589.
View Article
Google Scholar

[66] View Article

[67] Google Scholar

[ref20] 20. Stark JD, Banks JE. Population-level effects of pesticides and other toxicants on arthropods. Annu Rev Entomol. 2003; 48: 505–519. pmid:12221038
View Article
PubMed/NCBI
Google Scholar

[69] View Article

[70] PubMed/NCBI

[71] Google Scholar

[ref21] 21. Chi H, Liu H. Two new methods for the study of insect population ecology. Bull Inst Zool Acad Sinica. 1985; 24: 225–240.
View Article
Google Scholar

[73] View Article

[74] Google Scholar

[ref22] 22. Chi H. Life-table analysis incorporating both sexes and variable development rates among individuals. Environ Entomol. 1988; 17: 26–34.
View Article
Google Scholar

[76] View Article

[77] Google Scholar

[ref23] 23. Chi H, Su HY. Age-stage, two-sex life tables of Aphidius gifuensis (Ashmead) (Hymenoptera: Braconidae) and its host Myzus persicae (Sulzer) (Homoptera: Aphididae) with mathematical proof of the relationship between female fecundity and the net reproductive rate. Environ Entomol. 2006; 35: 10–21.
View Article
Google Scholar

[79] View Article

[80] Google Scholar

[ref24] 24. Zeng XY, He YQ, Wu JX, Tang YM, Gu J, Ding W, et al. Sublethal effects of cyantraniliprole and imidacloprid on feeding behavior and life table parameters of Myzus persicae (Hemiptera: Aphididae). J Econ Entomol. 2016; 109: 1595–1602. pmid:27247299
View Article
PubMed/NCBI
Google Scholar

[82] View Article

[83] PubMed/NCBI

[84] Google Scholar

[ref25] 25. Chen XW, Ma KS, Li F, Liang PZ, Liu Y, Guo TF, et al. Sublethal and transgenerational effects of sulfoxaflor on the biological traits of the cotton aphid, Aphis gossypii Glover (Hemiptera: Aphididae). Ecotoxicology. 2016; 25: 1841–1848. pmid:27670668
View Article
PubMed/NCBI
Google Scholar

[86] View Article

[87] PubMed/NCBI

[88] Google Scholar

[ref26] 26. Saska P, Skuhrovec J, Lukáš J, Chi H, Tuan SJ, Honěk A. Treatment by glyphosate-based herbicide alters life history parameters of the rose-grain aphid Metopolophium dirhodum. Sci Rep. 2016; 6: 27801. pmid:27302015
View Article
PubMed/NCBI
Google Scholar

[90] View Article

[91] PubMed/NCBI

[92] Google Scholar

[ref27] 27. Chu JX. Agricultural Entomology. Beijing: China Agricultural Press; 2009.

[ref28] 28. Wang SB, Chen B, Wang Y, Bu HM. Synthesis discussion of prevention and cure on wheat aphid and yellow dwarf. J Shanxi Agric Sci. 2003; 31: 69–71.
View Article
Google Scholar

[95] View Article

[96] Google Scholar

[ref29] 29. Gray SM, Bergstrom GC, Vaughan R, Simth DM, Kalb DW. Insecticidal control of cereal aphids and its impact on the epidemiology of the barley yellow dwarf luteoviruses. Crop Prot. 1996; 15: 687–697.
View Article
Google Scholar

[98] View Article

[99] Google Scholar

[ref30] 30. Brault V, Herrbach É, Reinbold C. Electron microscopy studies on luteovirid transmission by aphids. Micron. 2007; 38: 302–312. pmid:16750376
View Article
PubMed/NCBI
Google Scholar

[101] View Article

[102] PubMed/NCBI

[103] Google Scholar

[ref31] 31. Miao J, Du ZB, Wu YQ, Gong ZJ, Jiang YL, Duan Y, et al. Sub-lethal effects of four neonicotinoid seed treatments on the demography and feeding behaviour of the wheat aphid Sitobion avenae. Pest Manag Sci. 2014; 70: 55–59. pmid:23457039
View Article
PubMed/NCBI
Google Scholar

[105] View Article

[106] PubMed/NCBI

[107] Google Scholar

[ref32] 32. Moores GD, Gao XW, Denholm I, Devonshire AL. Characterisation of insensitive acetylcholinesterase in insecticide resistant cotton aphids, Aphis gossypii Glover (Homoptera: Aphididae). Pestic Biochem Physiol. 1996; 56:102–110
View Article
Google Scholar

[109] View Article

[110] Google Scholar

[ref33] 33. Chi H. TWOSEX-MSChart: a computer program for the age-stage, two-sex life table analysis. 2018; 2:20. Available from: http://140.120.197.173/Ecology/Download/TWOSEX-MSChart-B100000.rar
View Article
Google Scholar

[112] View Article

[113] Google Scholar

[ref34] 34. Efron B, Tibshirani RJ. An Introduction to the Bootstrap. Boca Raton, London, New York, Washington, D.C.: Chapman and Hall/CRC; 1994.

[ref35] 35. Reddy GVP, Chi H. Demographic comparison of sweetpotato weevil reared on a major host, Ipomoea batatas, and an alternative host, I. triloba. Sci Rep, 2015; 5: 11871. pmid:26156566
View Article
PubMed/NCBI
Google Scholar

[116] View Article

[117] PubMed/NCBI

[118] Google Scholar

[ref36] 36. Brandstätter E. Confidence intervals as an alternative to significance testing. Methods of Psychological Research Online. 1999; 4: 33–46. (Internet: http://www.ipn.uni-kiel.de/mpr/)
View Article
Google Scholar

[120] View Article

[121] Google Scholar

[ref37] 37. Huang YB, Chi H. Assessing the application of the Jackknife and Bootstrap techniques to the estimation of the variability of the net reproductive rate and gross reproductive rate: a case study in Bactrocera cucurbitae (Coquillett) (Diptera: Tephritidae). J Agric & Fore. 2012; 61: 37–45.
View Article
Google Scholar

[123] View Article

[124] Google Scholar

[ref38] 38. Qu YY, Xiao D, Li JY, Chen Z, Biondi A, Desneux N, et al. Sublethal and hormesis effects of imidacloprid on the soybean aphid Aphis glycines. Ecotoxicology. 2015; 24: 479–487. pmid:25492586
View Article
PubMed/NCBI
Google Scholar

[126] View Article

[127] PubMed/NCBI

[128] Google Scholar

[ref39] 39. Gerami S, Jahromi KT, Ashouri A, Rasoulian G, Heidari A. Sublethal effects of imidacloprid and pymetrozine on the life table parameters of Aphis gossypii Glover (Homoptera: Aphididae). Comm Appl Biol Sci. 2005; 70:779–785.
View Article
Google Scholar

[130] View Article

[131] Google Scholar

[ref40] 40. Nauen R, Koob B, Elbert A. Antifeedant effects of sublethal dosages of imidacloprid on Bemisia tabaci. Entomol Exp Appl. 1998; 88: 287–293.
View Article
Google Scholar

[133] View Article

[134] Google Scholar

[ref41] 41. Calabrese EJ, Baldwin LA. Hormesis: a generalizable and unifying hypothesis. Crit Rev Toxicol. 2001; 31: 353–424. pmid:11504172
View Article
PubMed/NCBI
Google Scholar

[136] View Article

[137] PubMed/NCBI

[138] Google Scholar

[ref42] 42. Cordeiro EM, de Moura IL, Fadini MA, Guedes RN. Beyond selectivity: are behavioural avoidance and hormesis likely causes of pyrethroid-induced outbreaks of the southern red mite Oligonychus ilicis? Chemosphere. 2013; 93: 1111–1116. pmid:23830118
View Article
PubMed/NCBI
Google Scholar

[140] View Article

[141] PubMed/NCBI

[142] Google Scholar

[ref43] 43. Guedes RN, Cutler GC. Insecticide-induced hormesis and arthropod pest management. Pest Manag Sci. 2014; 70: 690–697. pmid:24155227
View Article
PubMed/NCBI
Google Scholar

[144] View Article

[145] PubMed/NCBI

[146] Google Scholar

[ref44] 44. Drobne D, Blažič M, Van Gestel CA, Lešer V, Zidar P, Jemec A, et al. Toxicity of imidacloprid to the terrestrial isopod Porcellio scaber (Isopoda, Crustacea). Chemosphere. 2008; 71: 1326–1334. pmid:18190949
View Article
PubMed/NCBI
Google Scholar

[148] View Article

[149] PubMed/NCBI

[150] Google Scholar

[ref45] 45. Miao J, Reisig DD, Li GP, Wu YQ. Sublethal effects of insecticide exposure on Megacopta cribraria (Fabricius) nymphs: key biological traits and acetylcholinesterase activity. J Insect Sci. 2016; 16: 99; 1–6.
View Article
Google Scholar

[152] View Article

[153] Google Scholar

[ref46] 46. Azevedo-Pereira HMVS, Lemos MFL, Soares AMVM. Effects of imidacloprid exposure on Chironomus riparius Meigen larvae: linking acetylcholinesterase activity to behaviour. Ecotoxicol. Environ Saf. 2011; 74: 1210–1215. pmid:21511337
View Article
PubMed/NCBI
Google Scholar

[155] View Article

[156] PubMed/NCBI

[157] Google Scholar

[ref47] 47. Gong YH, Shi XY, Desneux N, Gao XW. Effects of spirotetramat treatments on fecundity and carboxylesterase expression of Aphis gossypii Glover. Ecotoxicology. 2016; 25: 655–663. pmid:26898726
View Article
PubMed/NCBI
Google Scholar

[159] View Article

[160] PubMed/NCBI

[161] Google Scholar

[ref48] 48. Wen YC, Liu ZW, Bao HB, Han ZJ. Imidacloprid resistance and its mechanisms in field populations of brown planthopper, Nilaparvata lugens Stål in China. Pestic Biochem Physiol. 2009; 94: 36–42.
View Article
Google Scholar

[163] View Article

[164] Google Scholar

[ref49] 49. Zhang YX, Yang YX, Sun HH, Liu ZZ. Metabolic imidacloprid resistance in the brown planthopper, Nilaparvata lugens, relies on multiple P450 enzymes. Insect Biochem Mol Biol. 2016; 79: 50–56. pmid:27793627
View Article
PubMed/NCBI
Google Scholar

[166] View Article

[167] PubMed/NCBI

[168] Google Scholar

[ref50] 50. Puinean AM, Foster SP, Oliphant L, Denholm I, Field LM, Millar NS, et al. Amplification of a cytochrome P450 gene is associated with resistance to neonicotinoid insecticides in the aphid Myzus persicae. PLoS Genet. 2010; 6: e1000999. pmid:20585623
View Article
PubMed/NCBI
Google Scholar

[170] View Article

[171] PubMed/NCBI

[172] Google Scholar

Figures

Abstract

Introduction

Materials and methods

Ethics statement

Insects

Insecticide and enzyme kits

Acute toxicity of imidacloprid on R. padi

Sublethal effects of imidacloprid on R. padi

Enzyme activity determination

Data analysis

Results

Acute toxicity of imidacloprid on R. padi

Sublethal effects of imidacloprid on biological parameters of R. padi

Sublethal effects of imidacloprid on enzyme activity of R. padi

Discussion

Supporting information

S1 Table. Spread sheet tables presenting supplementary data.

Acknowledgments

References