Introduction

In agroecosystems, insects often experience lethal effects when exposed to functional doses or residues of chemical insecticides (Desneux et al. 2005; 2007). These chemical insecticides have also been reported to induce sublethal effects on exposed arthropods (Desneux et al. 2007; Ullah et al. 2019c; Gul et al. 2021; 2023). These sublethal effects can significantly impact the biological traits and population dynamics of both directly exposed insects and their descendants (Ullah et al. 2019a; Ullah et al. 2020; Shi et al. 2022; Jia et al. 2022). The occurrence of lethal or sublethal effects in insects depends on several factors with the dose or concentration of insecticide being the most crucial determinate (Cutler. 2013; Decourtye et al. 2013). Though, the dose/concentration of insecticides is the main consideration for managing the target pest, biotic and abiotic factors which can cause spatiotemporal fluctuations in concentrations are underestimated (Desneux et al. 2005). Although the sublethal concentrations/doses affect the life-history traits of exposed insects, they may also result in boosting metabolic activities and, eventually, the growth of exposed organisms is accelerated (Rix and Cutler. 2022). This biological phenomenon is termed ‘hormesis’ i.e., stimulation at low concentrations/doses and inhibition at higher concentrations/doses (Cutler et al. 2022). The hormetic effects of sublethal concentrations and dosages of pesticides should be assessed as they may inadvertently lead to increased crop injury (Guedes et al. 2016).

The greenbug, Schizaphis graminum (Rondani) (Hemiptera: Aphididae), is one of the most economically important pests of wheat worldwide (Hullé et al. 2020). This key pest causes direct damage through sap feeding and indirect damage by transmitting several plant pathogenic viruses, including the barley yellow dwarf mosaic virus and the sugarcane mosaic virus (Hullé et al. 2020). Despite several options for pest management in general (Wang et al. 2021; Zhang et al. 2021; Nieri et al. 2022; Ullah et al. 2022), insecticide application remains an important tool that farmers easily use (Desneux et al. 2022; Kenis et al. 2023). Thiamethoxam is a neonicotinoid insecticide commonly used to control sap-sucking insect pests in various crops (Ullah et al. 2020; Zhang et al. 2022). This insecticide specifically binds to nicotinic acetylcholine receptors (nAChRs) in insect nervous systems, generating nerve stimulation, paralysis, and death (Tomizawa and Casida. 2005). Apart from lethal effects, insecticides, especially neonicotinoids, have sublethal effects on arthropod’s physiological and behavioral characteristics, such as lifespan, developmental period, fecundity, host finding, and feeding activity (Ullah et al. 2019b; Aeinehchi et al. 2021; Hafeez et al. 2022). These effects can be intergenerational, influencing offspring indirectly (Shi et al. 2022), resulting in changing communities and ecological services (Lu et al. 2012; Abd Allah et al. 2019). Hormetic effects caused by insecticides have recently been reported in melon aphids Aphis gossypii Glover (Hemiptera: Aphididae) following exposure to LC5 and LC15 of acetamiprid and imidacloprid (Ullah et al. 2019a; 2019b). The sublethal concentrations of nitenpyram, pirimicarb, and flonicamid enhanced fecundity in A. gossypii (Koo et al. 2015; Wang et al. 2017). Similar effects were noted for Myzus persicae (Sulzer) (Hemiptera: Aphididae) when treated to the LC25 of flupyradifurone (Tang et al. 2019). In addition to other effects, sublethal concentrations of insecticides may interfere with the feeding behavior of target insect pests (Miao et al. 2014; Zeng et al. 2016; Yuan et al. 2017).

The age-stage, two-sex life table is used for studying the lethal and intergenerational, transgenerational or multi-generational sublethal effects of insecticides on insects (e.g., Gul et al. 2021; 2023; Chi et al. 2020; 2023a). In contrast to the traditional female age-specific life table analysis, this approach accounts for stage differentiation and provides more accurate estimates of various life table parameters (Chi et al. 2020; Ding et al. 2021; Chi et al. 2022a; 2022b). Additionally, digital monitoring of insect feeding by the Electrical Penetration Graph (EPG) system is a promising tool (Tariq et al. 2017; Yuan et al. 2017; Milenovic et al. 2019). The EPG technique has been widely used for the detailed investigation of the feeding behavior of piercing-sucking insects. To determine a suitable plant for feeding, aphid do several probing attempts (Sauge et al. 2002). Cho et al. (2011) and Gul et al. (2023) reported that the sublethal concentrations of flonicamid and thiamethoxam affect the feeding behavior of aphids. The LC30 of flonicamid and imidacloprid significantly decreased the total duration of phloem ingestion of A. gossypii (Koo et al. 2015). Miao et al. (2014) showed that the LC10 and LC50 of imidacloprid, dinotefuran, thiacloprid and thiamethoxam cause a higher percentage of no probing phase and shorter phloem sap ingestion phase on treated wheat plants. These studies showed that the sublethal concentrations of insecticides significantly affect the feeding behavior of targeted insects.

In this study, we determined the toxicity of thiamethoxam against S. graminum and calculate the LC5 and LC10 concentrations. We used these concentrations to investigate the hormetic effects of thiamethoxam on survival, development, fecundity, and population projection of S. graminum using an age-stage, two-sex life table approach. Furthermore, the feeding behavior of S. graminum has also been investigated following exposure to the LC5 and LC10 concentrations of thiamethoxam.

Material and methods

Study insect

The apterous S. graminum, originally collected from the wheat field, was reared for more than two years at the National Agricultural Research Center (NARC), Islamabad, Pakistan. The parthenogenetic colony of S. graminum was maintained on wheat seedlings without any insecticide exposure under laboratory conditions with a temperature of 18 ± 2 °C, 60 ± 5% RH, and a photoperiod of 16:8 L: D.

Bioassays

The thiamethoxam (Actara® 25 WG) insecticide was provided by Syngenta Pakistan Ltd. To determine the toxicity, thiamethoxam was diluted into five test concentrations (40, 20, 10, 5, and 2.5 mg L−1) from the corresponding stock solution. All serial concentrations were applied in bioassays immediately after preparation. The wheat plants at the leaf stage were sprayed with five concentrations separately using hand sprayers until run-off (adaxial and abaxial leaf sides). In the control group, the plants were sprayed with distilled water. The treated wheat plants were kept to dry at room temperature. Each insecticide concentration and control has three replicates, and thirty adult apterous aphids were used per replicate. The treated wheat plants containing aphids were kept under laboratory conditions with a temperature of 18 ± 2 °C, 60 ± 5% RH, and a photoperiod of 16:8 L: D. The mortality was recorded at 48 h after exposure to thiamethoxam. Aphids not moving when pushed gently with a soft brush were considered dead.

Sublethal effects of thiamethoxam on Schizaphis graminum (F0)

We employed the sublethal concentrations (LC5 and LC10) of thiamethoxam to elucidate their impact on directly exposed S. graminum (F0) after likely occurring due to insecticide degradation under field conditions. The healthy wheat plants were sprayed with the LC5 (2.259 mg L−1) and LC10 (3.057 mg L−1) values calculated by a log-probit model and determined using the previously described bioassay using a hand sprayer until run-off (adaxial and abaxial leaf sides). In the control treatment, the wheat plants were sprayed with distilled water. The wheat plants that had been treated were allowed to dry at room temperature. Apterous adult aphids were transferred to the insecticide-treated and control wheat plants. The treated wheat plants were kept under laboratory conditions with a temperature of 18 ± 2 °C, 60 ± 5%, and a photoperiod of 16:8 L:D. After 48 h treatment, forty survived, and healthy aphids were individually transferred to micro cages containing insecticide-free wheat plants. Each aphid was considered a single replicate. The longevity and fecundity of S. graminum were recorded daily. After counting, the newly born nymphs were removed from the cage. The data were continuously recorded until the death of all aphids.

Intergenerational impact of thiamethoxam on Schizaphis graminum (F1)

The intergenerational impact of LC5 and LC10 of thiamethoxam on the succeeding parthenogenetically F1 generation of S. graminum was checked following the same experimental setup. Forty newly-born nymphs from F0 parents - the F1 individuals - were randomly selected and transferred to clean micro cages containing insecticide-free fresh wheat plants individually. Each aphid was considered a single replicate. The survival and developmental duration of F1 aphids were recorded daily. The daily fecundity (nymphs per aphid) was counted and removed daily until death. The experiments were performed under standard laboratory conditions as described above.

Electropenetrography of Schizaphis graminum feeding behavior

The feeding behavior of adult S. graminum on wheat plants treated with the LC5 and LC10 of thiamethoxam was monitored using an eight-channel DC-EPG (Wageningen University, The Netherlands). Moreover, we investigated the intergenerational effects on the feeding behavior of progeny generation adults whose parents were treated with the LC5 and LC10 of thiamethoxam. Briefly, the wheat plants were sprayed with the LC5 and LC10 using a hand sprayer until run-off (adaxial and abaxial leaf sides). Plants were sprayed with distilled water for blank controls. The treated plants were air-dried for 2 h at room temperature before experiments. Adult aphids were starved for approximately 1 h between wiring and the beginning of the EPG experiment. After starvation, aphids were individually connected via their dorsum to a gold wire (18 μm in diameter and 6–8 cm in length) using a small drop of high purity silver conductive paint. The insect attached to the gold wire was then carefully placed on the treated wheat plants. The gold wire was connected to Giga-8 DC-EPG amplifier with 109Ω input resistance and an adjustable plant voltage. A copper wire (2 mm in diameter and 5 cm in length) which served as a plant electrode, was inserted into the pot soil to provide voltage. The waveforms were recorded simultaneously from eight plants with alternate channels of water or thiamethoxam-treated plants. To avoid external electrical noises, the experiments were conducted in an electrically earthed Faraday cage (2 × 2 × 4 feet, aluminum frame with a steel base) at 18 °C and 60–65% RH under continuous light for eight hours using PROBE 3.4 software (Wageningen Agricultural University, Wageningen, The Netherlands). Freshly treated wheat plants and aphids were used for each replication. EPGs for each treatment were recorded for 8 h, which were used for final data analysis.

The EPG recordings were analyzed using Stylet+ Software. The variables of EPG were processed using EPG-Excel Data Workbook according to EPG ParProc. The EPG waveforms correlated with the probing activity were described as Np: Total duration of non-probing, Pr: Mean duration of probing, C: Total duration of intercellular stylet pathway, G: Total duration of xylem ingestion, E1: Total duration of salivary secretion into the sieve element, E2: Total duration of phloem sap ingestion and concurrent salivation.

Data analysis

The LC5, LC10, and LC50 of thiamethoxam were calculated using log-probit model in PoloPlus 2.0 (LeOra Software Inc., Berkeley, CA). The electropenetrography (EPG) data were statistically analyzed using a one-way analysis of variance with Tukey’s post hoc test (IBM, SPSS Statistics, version 22).

Life table data analysis

The raw data of control, LC5, and LC10 treated F0 cohorts and their progeny (F1) were analyzed using the age-stage, two-sex life table method (Chi, 1988; Chi and Liu, 1985; Chi et al. 2020; Chi et al. 2023a). The development time, female longevities, reproductive days (RPd), adult pre-reproductive period (APRP), total pre-reproductive period (TPRP), and fecundity (F) (nymphs/female), as well as the demographic traits including the intrinsic rate of increase (r), finite rate of increase (λ), net reproductive rate (R0), and mean generation time (T) were determined using TWOSEX-MSChart computer program (Chi, 2023b; Chi et al. 2022a, 2022b). The standard errors were calculated by 100,000 bootstrap replicates (Huang and Chi. 2012; Amir-Maafi et al. 2022). The differences between the demographic parameters of control, LC5, and LC10 treated groups were determined using the paired bootstrap test at 5% significance level based on the confidence interval of difference (Wei et al. 2020). Details of the life table analysis were given as supplementary file.

Population projection

Projections were made using the TIMING- MSChart program (Chi 2023c) based on the method of Chi and Liu. (1985) and Chi (1990). The population projection of S. graminum began with 10 newborn nymphs for each concentration, including the control under the assumption of no suppression by biotic and abiotic factors. It was projected for 50 days, a duration typically allowing S. graminum to establish and cause economically significant damage in winter wheat production. We conducted a comprehensive analysis using 100,000 bootstrap results of the finite rate of increase (λ). Within this dataset, we identified the 2.5th and 97.5th percentiles, which corresponded to the 2500th and 97,500th sorted bootstrap samples, respectively. Subsequently, we utilized the life table samples from the bootstrap analysis that generated the 2.5th and 97.5th percentiles of the finite rate of increase (λ) to simulate the population’s growth over a 50-day period. This process allowed us to assess and visualize the variability and uncertainty in the projected populations, providing valuable insights into the confidence intervals associated with our results (Huang et al. 2017).

Results

Toxicity of thiamethoxam on Schizaphis graminum

The toxicity results of thiamethoxam against S. graminum adults after exposure for 48 h showed that the LC50 value was 8.89 mg L−1 (95% confidence interval [CI] 7.811–10.077 mg L−1). The LC5 and LC10 values were found as 2.259 mg L−1 (95% CI: 1.657–2.851 mg L−1) and 3.057 mg L−1 (95% CI 2.360–3.725 mg L−1), respectively (Table 1).

Table 1 Toxicity of thiamethoxam against adult Schizaphis graminum after 48 h exposure
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Impact of LC5 and LC10 of thiamethoxam on parental aphids (F0)

The 48-h (48 h) LC5 and LC10 of thiamethoxam significantly affected the longevity and fecundity of adult S. graminum (Table 2). The longevity and fecundity of S. graminum significantly decreased following exposure to the LC5 and LC10 of thiamethoxam as compared to control (P < 0.05). The number of the reproductive days were lowest on LC10 of thiamethoxam treated individuals (Table 2, P < 0.05).

Table 2 Adult longevity, fecundity and reproductive days of the control, LC5 and LC10 of thiamethoxam treated F0 generation of Schizaphis graminum
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Developmental duration and adult longevity of F1 Schizaphis graminum

The intergenerational sublethal effects on F1 S. graminum whose parents (F0) were treated with the LC5 and LC10 of thiamethoxam are shown in Table 3. Results showed that the developmental period of 1st instar significantly decreased (P < 0.05) with the LC5 of thiamethoxam, while no effects were observed for the LC10 group as compared to control (Table 3). The developmental duration of 3rd instar S. graminum was significantly reduced (P < 0.05) at LC5 concentration compared to control. However, no effects were noted at the LC10 (P > 0.05). Similarly, the 4th instar duration was also decreased (P < 0.05) in LC5 treated group as compared to LC10 and control groups (Table 3). The duration of 2nd instar aphids was not affected at both concentrations (P > 0.05). Correspondingly, the pre-adult period of F1 S. graminum was significantly decreased (P < 0.05) when the parental aphids were exposed to the LC5 of thiamethoxam compared to LC10 and control groups. In contrast, the adult longevity of F1 aphids was significantly increased (P < 0.05) at the LC5, while no effects were observed at LC10 as compared to control (Table 3). The age-stage specific survival rate (sxj) shows the probability that a newly born nymph of S. graminum will survive to age x and stage j (Fig. S1). Various overlaps were observed among the LC5, LC10, and control due to the differences in the developmental and adult stages of S. graminum.

Table 3 Duration (days) of different developmental stages of the control and F1 generation of Schizaphis graminum, whose parents (F0) were treated with LC5 and LC10 of thiamethoxam
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Fecundity and life table parameters of F1 Schizaphis graminum

The age-specific survival rate (lx), age-specific fecundity (mx) and the age-specific maternity (lxmx) curves for the LC5, LC10, and control groups were presented in Fig. 1. The lx, mx and lxmx parameters were affected in the LC10 while stimulated in the LC5 of thiamethoxam as compared to control. The age-stage specific survival rate (exj) shows the expected duration of an individual aphid of age x and stage j that will survive after the age x (Fig. S2). The curves represent that the F1 generation of S. graminum is expected to live longer in the LC5 treatment while shorter in the LC10 of thiamethoxam as compared to control. The age-stage reproductive value (vxj) curves show the as the contribution of individuals of age x and stage j to the future population (Fig. S3). The maximum vxj values were noted in the LC5 treated insects, whereas the minimum values were observed in LC10 of thiamethoxam as compared to the control.

Fig. 1
figure 1

Population age-specific survival rate (lx), age-specific fecundity (mx) and the age-specific maternity (lxmx) for F1 generation Schizaphis graminum descending from F0 individuals treated with the LC5 and LC10 of thiamethoxam and control

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The intergenerational impact of thiamethoxam on the reproduction and life table parameters of F1 aphids whose parents were treated with the LC5 and LC10 concentrations are shown in Table 4. The results indicated that the net reproductive rate (R0) of F1 aphids at LC5 was 1.2 times higher than that of the control (P < 0.05), whereas no statistically significant difference was observed at the LC10 compared to the control (P > 0.05). Similarly, the r and λ were significantly increased (P < 0.05) in F1 individuals at the LC5 treatment compared to the control. However, no significant effects (P > 0.05) were noted in the LC10 treatment (Table 4). The T value was dramatically decreased (P < 0.05) at the LC5 of thiamethoxam compared to the LC10 and control groups. The fecundity (F) of F1 aphids was substantially enhanced (P < 0.05) only at the LC5 of thiamethoxam, while the reproductive days (RPd) were dramatically increased at both concentrations as compared to control (P < 0.05). Compared to control, the adult pre-reproductive period (APRP) and total pre-reproductive period (TPRP) were significantly reduced (P < 0.05) at the LC5, while no effects were observed at the LC10 of thiamethoxam (Table 4).

Table 4 Reproduction and life table parameters of control and F1 generation of Schizaphis graminum, whose parents (F0) were treated with LC5 and LC10 of thiamethoxam
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Population projection

The original, 2.5th, and 97.5th percentiles of population projections of the F1 progeny of S. graminum produced by LC5 and LC10 concentrations of thiamethoxam treated populations and control group are plotted in Fig. 2. The highest total population size was found in the population produced from LC5 of thiamethoxam and was projected to surpass 9.0 × 108 individuals after 50 days. The population produced from LC10 of thiamethoxam treated S. graminum yielded the lowest population size estimate with ~1.7 × 107, while the control group was ~2.4 × 107 after 50 days.

Fig. 2
figure 2

Total population size (Nt) after projection of control and F1 progeny of Schizaphis graminum produced by LC5 and LC10 of thiamethoxam treated parents and control for a 50-day period by using life table data. (All data are in log base 10 and the shaded areas represent the limits of the 95% CIs based on the 2.5 and 97.5% percentiles of λ, finite rate of increase)

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Sublethal effects of thiamethoxam on feeding behavior of F0 and F1 S. graminum

The LC5 and LC10 of thiamethoxam significantly affected the feeding behavior of directly exposed adult S. graminum as compared to the control insects (Table 5). The waveforms recorded from S. graminum on wheat plants treated with the LC5 and LC10 of thiamethoxam are shown in Figs. 3, S4. Results showed that the Np durations (total duration of non-probing) of the LC5 and LC10 treatments were 1610 and 1305 s, respectively, which were significantly (P < 0.05) longer than the control group (460 s). The mean duration of Pr (mean duration of probing) was substantially decreased in the LC5 (19842 s) and LC10 (19211 s) concentrations of thiamethoxam as compared to control (20984 s) (P < 0.05). The total duration of C (total duration of intercellular stylet pathway) was 7653 s in LC5 and 8323 s in LC10 while the total duration of E1 (total duration of salivary secretion into the sieve element) was 1465 s in LC5 and 1238 s in LC10 treatments, which are significantly (P > 0.05) longer than control aphids (Table 5). Moreover, the total duration of E2 (total duration of phloem sap ingestion and concurrent salivation) substantially (P > 0.05) increased in the LC5 (9665 s) and LC10 (7134 s) treatments as compared to control (14969). No significant differences (P > 0.05) were observed in total duration of G (total duration of xylem ingestion) among the thiamethoxam treated insects and control (Table 5).

Table 5 Sublethal effects of thiamethoxam on the probing and feeding behavior of Schizaphis graminum on wheat plants treated with the LC5 and LC10 concentrations and control
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Fig. 3
figure 3

EPG waveforms recorded from Schizaphis graminum on wheat plants treated with the LC5 and LC10 of thiamethoxam and control. The EPG waveforms were described as Np: Total duration of non-probing, Pr: Mean duration of probing, C: Total duration of intercellular stylet pathway, G: Total duration of xylem ingestion, E1: Total duration of salivary secretion into the sieve element, E2: Total duration of phloem sap ingestion and concurrent salivation

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The intergenerational sublethal effects on the probing and feeding behavior were checked on F1 adult aphids whose parents (F0) were treated with the LC5 and LC10 of thiamethoxam (Table 6). The waveforms recorded from progeny generation S. graminum (F1) descending from parental aphids treated with the LC5 and LC10 of thiamethoxam are shown in Fig. 4. Results showed that the Np duration of F1 individuals was 463.8 sec in the LC5 treated group, which is significantly shorter than the LC10 (985.7 s) and control groups (1000.2 s) (P < 0.05). The total duration of Pr was substantially longer (P < 0.05) in the LC5 treatment (21028 s) as compared to LC10 (19945 s) and control (20419 s). Furthermore, the total duration of E2 in the LC5 treated group was 18,452 s which was significantly (P < 0.05) longer than the LC10 (14,162 s) and control aphids (14,222 s) (Table 6). The total duration of C, G and E1 were statistically same among the thiamethoxam treated aphids and control (P > 0.05) (Table 6).

Table 6 Intergenerational impact of thiamethoxam on the probing and feeding behavior of Schizaphis graminum (F1) whose parents were treated with the LC5 and LC10 concentrations and control
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Fig. 4
figure 4

EPG waveforms recorded from progeny generation Schizaphis graminum (F1) descending from parental aphids treated with the LC5 and LC10 of thiamethoxam. The EPG waveforms were described as Np: Total duration of non-probing, Pr: Mean duration of probing, C: Total duration of intercellular stylet pathway, G: Total duration of xylem ingestion, E1: Total duration of salivary secretion into the sieve element, E2: Total duration of phloem sap ingestion and concurrent salivation

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Discussion

In this study, we investigated the sublethal and intergenerational effects of thiamethoxam on two consecutive generations (F0 and F1) of S. graminum. The results demonstrated that thiamethoxam displayed high toxicity against S. graminum, with an LC50 of 8.89 mg/l following 48-h treatment. In addition to its lethal effects, thiamethoxam induces intergenerational sublethal and hormetic effects on the biological parameters of the exposed S. graminum. Similar effects have also been recorded in A. gossypii (Ullah et al. 2020). These results suggested that the LC5 and LC10 concentrations may be critical for managing S. graminum in field conditions.

The current study shows that the longevity and fecundity of adult S. graminum (F0) were reduced following exposure to the LC5 and LC10 of thiamethoxam for 48 h. Our results align with Ma et al. (2022) who demonstrated that the longevity and fecundity of parental adult A. gossypii (F0 generation) significantly declined when treated with LC10 of afidopyropen. Likewise, Ullah et al. (2019a) reported decreased longevity and fecundity of A. gossypii when directly exposed to the LC5 and LC15 of imidacloprid. The negative consequences, such as shorter lifespan and decreased fertility, were also observed in M. persicae when treated with flupyradifurone at sublethal concentrations (Tang et al. 2019). The total longevity and fecundity of S. graminum were significantly reduced following exposure to acetamiprid (Vakhide and Safavi. 2014). Cui et al. (2018) also reported decreased longevity and fecundity when parental A. gossypii (F0) were treated with the sublethal concentration of cycloxaprid. These results showed that along with lethal effects, the sublethal concentrations of insecticides greatly affect the adult lifespan and fertility of the surviving aphids. Therefore, it is crucial to investigate the sublethal effects of commonly used insecticides on target insects to better understand their efficacy even after degradation due to biotic and abiotic constraints.

On the other hand, the developmental stages of F1 S. graminum were positively affected when the parental aphids (F0) were exposed to the LC5 of thiamethoxam. Results showed that the developmental duration of 1st, 3rd, and 4th instar of F1 S. graminum was significantly decreased at the LC5 as compared to LC10 treated group and control. The pre-adult stage was significantly shorter in progeny aphids (F1) when parental generation (F0) was treated with the LC5 of thiamethoxam compared to LC10 and control groups. In contrast, the adult longevity of F1 S. graminum was substantially prolonged when the parental aphids (F0) were treated with the LC5, while no effects were observed for the LC10 as compared to control. These results indicated that the LC5 of thiamethoxam positively affects the development and overall lifespan of S. graminum following parental adults after 48 h exposure. Ullah et al. (2019a) reported decreased developmental duration of 4th instar and pre-adult stage of F1 A. gossypii when parental aphids (F1) were treated with the LC5 and LC15 of imidacloprid. The developmental duration of 3rd and 4th instars and pre-adult stages of M. persicae was significantly decreased following 48 h exposure to the LC25 of flupyradifurone (Tang et al. 2019). The LC15 of thiamethoxam significantly reduced the 4th instar duration of F1 A. gossypii (Ullah et al. 2020). Yuan et al. (2017) also reported that the sublethal concentrations of cycloxaprid significantly decreased the developmental duration of F1 generation A. gossypii. The adult longevity of progeny generation of A. gossypii (F1) was significantly prolonged when parental generation (F0) was exposed to the LC5 and LC15 of imidacloprid and thiamethoxam (Ullah et al. 2019a; 2020). Tang et al. (2019) reported that the longevity of F1 and F2 generations of M. persicae were significantly extended when the parental aphids (F0) were treated with the LC25 of flupyradifurone. The male and female longevity of Nilaparvata lugens (Stål) (Hemiptera: Delphacidae) was significantly increased following exposure to the LC20 of nitenpyram for over 6 successive generations (Gong et al. 2022). The results of the current study and previous findings suggested that the sublethal concentrations of insecticides speed-up the developmental stages as well as increased the total longevity of target insect pests that ultimately enhance and support the pest outbreak in the field and causes severe damage to crops.

In the present study, the intergenerational hormetic effects were observed in S. graminum after exposure of the parental aphids to the LC5 of thiamethoxam compared to the LC10 and untreated aphids. For example, the female fecundity (F) and reproductive days (RPd) were significantly increased, while the adult pre-reproductive period (APRP) and total pre-reproductive period (TPRP) were markedly decreased in the progeny generation (F1) of LC5 treated group as compared to the LC10 and control aphids. Consequently, the demographic parameters, i.e., intrinsic rate of increase (r), finite rate of increase (λ) and net reproductive rate (R0), were significantly increased in the LC5 treatment as compared to LC10 and control. These changes in the life history traits of S. graminum indicated that the intergenerational hormetic effects occurred after 48 h exposure of parental aphids to the LC5 of thiamethoxam. This hormetic response occurred in S. graminum without any fitness tradeoffs following exposure to the LC5 and LC10 of thiamethoxam. Concurrent hormetic responses of multiple traits have been reported in A. gossypii exposed to thiamethoxam, imidacloprid and acetamiprid (Ullah et al. 2019a; Ullah et al. 2019b; Ullah et al. 2020), M. persicae exposed to flupyradifurone, acetamiprid, and imidacloprid (Ayyanath et al. 2013; Tang et al. 2019; Sial et al. 2018). Gong et al. (2022) examined transgenerational hormesis in brown planthopper (N. lugens) after six generations of 96 h exposure to LC20 nitenpyram. The pre-adult developmental duration and T were significantly decreased in F-Sub6 strain of N. lugens when subjected to the LC20 of nitenpyram (Gong et al. 2022). A similar phenomenon was also observed in our current study; the pre-adult developmental duration and T of S. graminum were substantially shortened in the LC5 treated group compared to the control. No significant effects were noted for the LC10 concentration of thiamethoxam. The population size of S. graminum projected at 50 days post-exposure was larger in the LC5 treated group than in the LC10 and control groups. Priming hormesis may be necessary for agricultural insect pests likely to encounter multiple and successive low and sublethal stress levels (Rix et al. 2016; Cutler et al. 2022). Overall, the results of the present study strongly demonstrated that exposure to the LC5 and LC10 of thiamethoxam caused intergenerational hormetic effects on the demographic characteristics of S. graminum. This increased reproduction and longevity might causes the pest outbreak under field contexts which ultimately increase crop damage.

In addition to other parameters, we investigated the feeding behavior of parental and progeny S. graminum using electric penetration graph recordings (EPG) after exposure of F0 aphids to the LC5 and LC10 of thiamethoxam. Results showed that the total duration of non-probing (Np), total duration of intercellular stylet pathway (C), and total duration of salivary secretion into the sieve element were significantly increased, while mean duration of probing (Pr) and total duration of phloem sap ingestion and concurrent salivation (E2) were dramatically decreased in F0 adults following exposure to the LC5 and LC10 of thiamethoxam. These results demonstrated that aphids need more time to search appropriate nutritional sites when plants are exposed to the LC5 and LC10 of thiamethoxam. Similar results were shown by Miao et al. (2014) that the no probing phase was increased while the phloem sap ingestion phase was decreased in Sitobion avenae (Fabricius) (Hemiptera: Aphididae) on the wheat plants treated with LC10 and LC50 of thiamethoxam, imidacloprid, dinotefuran, and thiacloprid. Tariq et al. (2017) reported that inhibition of ingestion was dose-dependent, i.e., the increasing concentrations of flonicamid significantly enhanced the mean duration of non-probing phases while strongly inhibited the ingestion phases in cotton leafhopper, Amrasca biguttula Ishida (Hemiptera: Cicadellidae). The total duration of phloem sap ingestion and concurrent salivation (E2) were substantially reduced in F0 and F1 aphids after exposure to the sublethal concentrations of flonicamid (Gul et al. 2023). The LC30 of cyantraniliprole and imidacloprid significantly increased the total durations of intercellular stylet pathway (C) and mechanical probing difficulties (F) when green peach aphids feed on the treated tobacco plants (Zeng et al. 2016). The increasing concentrations of flonicamid and imidacloprid substantially increased the non-penetration phases (NP) and decreased the salivation (E1) and sap-feeding (E2) durations in A. gossypii (Koo et al. 2015). The LC40 of cycloxaprid had a negative impact on the phloem ingestion phases of A. gossypii (Yuan et al. 2017). The sublethal concentrations of cycloxaprid dramatically enhanced the non-probing durations and strongly inhibited the phloem ingestion phases of the treated S. avenae (Cui et al. 2012). All these results demonstrated that sublethal concentrations of insecticides negatively impact the survived sap-sucking insect pests. Interestingly, the total duration of Np was significantly decreased, while the total duration of E2 were significantly increased in the progeny generation (F1) following exposure of the parental aphids to the LC5 of thiamethoxam. Our results showed that the sublethal concentrations of thiamethoxam affect the feeding behavior of the directly exposed aphids (F0), while signifacantly increased the feeding behavior of the progeny generation. Here, we showed that the decreased longevity and fecundity of F0 aphids might be due to the direct effects of sublethal concentrations of insecticides on their feeding behavior, while enhanced reproduction and longevity may be due to the increased feeding behavior of F1 individuals that ultimately validated the hormetic effects. However, future studies are needed to investigate the in-depth mechanisms underlying the observed hormetic effects.

Conclusion

Overall, our results show the LC5 and LC10 of thiamethoxam significantly affect the life span, fecundity, and feeding behavior of directly exposed F0 aphids. However, the LC5 concentration induces intergenerational hormetic effects on the biological parameters and feeding behavior of progeny generation (F1) of S. graminum that could increase crop damage. To the best of our knowledge, the present study is the only one determining thiamethoxam-induced intergenerational hormetic effects on the demographic parameters and feeding behavior of S. graminum. However, future studies should be conducted to investigate the multi-generational hormetic effects of thiamethoxam on S. graminum in field context.