Introduction

The cotton aphid or melon aphid, Aphis gossypii Glover (Hemiptera: Aphididae), is one of the most economically important sap-sucking insect pests worldwide. It causes serious economic damage through direct feeding and indirectly via virus transmission and contamination of honeydew (Hullé et al. 2020). Although several methods have been developed and used to control agricultural pests (Ragsdale et al. 2011; Jactel et al. 2019; Zhang et al. 2021; Monticelli et al. 2022; Verheggen et al. 2022), the control of A. gossypii in China has largely depended on chemical control. Thiamethoxam is a second-generation neonicotinoid insecticide widely used to control sap-sucking insect pests (Ullah et al. 2020; Zhang et al. 2022). This insecticide binds to nicotinic acetylcholine receptors (nAChRs) in the nervous system, producing nerve stimulation, paralysis, and insect death (Tomizawa & Casida. 2005).

In agroecosystems, insects are exposed to sublethal concentrations due to misapplication or degradation of chemical insecticides due to biotic or abiotic factors (Desneux et al. 2005, 2007). After degradation, the residues of pesticides cause sublethal effects on the exposed arthropods as well as induce resistance development (Ullah et al. 2019c; Gul et al. 2021; Pires Paula et al. 2021). Sublethal effects are defined as the physiological or behavioral effects on individuals that survived following exposure to the sublethal or lethal dose/concentrations of pesticides (Desneux et al. 2007). The sublethal effects directly affect the life-history parameters of survived insects and their descendants (Ullah et al. 2019a, 2020; Jia et al. 2022; Shi et al. 2022). However, several factors, such as dose/concentration, affect these sublethal effects of insecticides on the exposed insects (Cutler 2013; Decourtye et al. 2013). The dose/concentrations of insecticides could boost the exposed individuals' metabolic activities, ultimately stimulating insect growth parameters (Rix & Cutler. 2022; Wang et al. 2022). Stimulation at low dose/concentrations and inhibition at higher dose/concentrations are termed hormesis phenomena (Cutler et al. 2022). Therefore, sublethal effects are crucial for checking the overall effects of any insecticides on target or non-target pests (Guedes et al. 2016). Besides lethal effects, insecticides have sublethal effects on the directly exposed arthropod's physiological and behavioral traits, such as lifespan, developmental period, fertility, and feeding activity (Ullah et al. 2019b; Aeinehchi et al. 2021; Hafeez et al. 2022). These sublethal effects can be transgenerational, affecting offspring and ultimately changing the communities and ecological services (Lu et al. 2012; Abd Allah et al. 2019). Ullah et al. (2019a, b) evaluated hormesis effects in A. gossypii after exposure to low lethal and sublethal concentrations of imidacloprid and acetamiprid (Ullah et al. 2019a, 2019b). Reproductive hormesis was also reported in A. gossypii following treatment with flonicamid, pirimicarb, and nitenpyram (Koo et al. 2015; Wang et al. 2017). Furthermore, the sublethal concentrations of imidacloprid, flupyradifurone, and precocene cause similar hormetic effects in Myzus persicae (Sulzer) (Hemiptera: Aphididae) (Tang et al. 2019; Yu et al. 2010; Ayyanath et al. 2015).

Life table analysis is a valuable tool for studying how biotic and abiotic factors influence the life history data of pests at population level (Chi et al. 2020; 2023). Up to now, the age-stage, two-sex analysis has been widely employed to examine the lethal, sublethal, transgenerational, and hormesis effects of insecticides on insect pests (Liu et al. 2022; Gul et al. 2023; Ju et al. 2023).

Therefore, our objectives were to investigate the sublethal effects of thiamethoxam on the biological characteristics of A. gossypii adults referred to as the F0 generation and to explore its subsequent transgenerational effects on the progeny F1 generation by utilizing the age-stage, two-sex life table analysis approach. The results showed that the fecundity, longevity, and reproductive days of the parental generation (F1) of A. gossypii significantly decreased at the LC5 and LC10 of thiamethoxam. Moreover, the sublethal concentrations of thiamethoxam significantly increased the longevity, fecundity, and key demographic parameters such as intrinsic rate of increase, finite rate of increase and reproductive days of F1 generation. Overall, this study showed the sublethal and transgenerational effects of thiamethoxam on cotton aphids that could be effective in IPM programs targeting this key pest.

Material and methods

Experimental insect and insecticide

The cotton aphid, Aphis gossypii population used in this research was collected from cotton fields in the Xinjiang Uygur Autonomous Region of China in 1999. The laboratory has successfully maintained the individuals for a period exceeding 15 years, with the regular inclusion of newly obtained individuals from the field every 2 years. Throughout this period, the susceptible population of A. gossypii has been kept without any insecticide exposure since their initial collection. The cotton plant, Gossypium hirsutum (L.), was used to raise A. gossypii. All experiments were conducted in a climatic chamber under controlled environmental conditions (22 ± 1 °C, 70 ± 10% R.H., 16:8 L:D).

Bioassays

The toxicity of thiamethoxam against A. gossypii was employed using a leaf-dipping technique. Thiamethoxam was diluted into six concentrations from the associated stock solution (highest concentration) to assess the toxicity. The cotton leaves were dissected into round discs with a diameter of 20 mm using a sharpened steel punch. Cotton leaf discs were dipped in the thiamethoxam concentrations or distilled water (control) for 15 s (Ma et al. 2022). The treated leaf discs were set on disposable PE gloves and air-dried at room temperature. All treated leaf discs were put upside down on 2% (w/v) agar substrates in 12-well cell culture plates. The apterous adult cotton aphids were gently put on leaf discs using a camel hair brush, and the plates were coated with Chinese art paper (Xuan paper) to keep them from escaping. The treatment was repeated three times for each concentration, with at least 30 aphids used in each replicate. The mortality was checked at 48 h after exposure to thiamethoxam. The aphids were considered dead if not moving when pushed gently with a soft brush. The LC5 and LC10 values were calculated using PoloPlus 2.00 (LeOra Software Inc., Berkeley, CA).

Sublethal effects of thiamethoxam on life-history traits of the F0 generation

Three hundred apterous adult cotton aphids were introduced on fresh cotton plants. After 24 h, all adults were removed, and the newborn nymphs were retained until they developed into apterous adult aphids. This procedure ensured all aphids were the same age (and growth stage) at the initial exposure stage to the insecticide. These adult aphids were subsequently used in the experiment as the F0 generation. Thiamethoxam was diluted to the LC5 and LC10 with distilled water. Cotton leaf discs (20 mm) were immersed for 15 s in thiamethoxam concentrations (LC5 and LC10) or distilled water (control). Each treated leaf disc was put on a plastic sheet to air dry at room temperature. The dried leaf discs were put on agar again in the 12-well cell-culture plates. The apterous adults were subsequently placed onto the cotton leaf discs and coated with filter paper to avoid escape. The cell plates were placed in the incubator. After 48 h, 40 alive aphids were individually transferred from each group (LC5, LC10, and control) onto new 20 mm cotton leaf discs without any insecticide. Throughout the experiment, fresh cotton leaf discs free of insecticide were substituted every 2–3 days. The survival, development, and fecundity were monitored every day. The newly born nymphs were counted daily and removed until the adult aphids reached the end of their life span.

Transgenerational effects of thiamethoxam on biological parameters of the progeny generation

Biological parameters were obtained by using same method described in the previous section from F1 generation, whose parents were sprayed LC5 and LC10 of thiamethoxam and control group. According to the preceding description, these aphids were individually kept on cotton leaf discs without insecticide. This process was carried out on 40 newly born F1 progeny for the thiamethoxam treatments and the control. The life table parameters, including fecundity, development, and survival rate of the F1 aphids, were monitored daily. Daily counts and removals of the newborn nymphs ensured that only adult aphids were left. The fresh cotton leaf discs free of insecticide were replaced every 2–3 days until the adult died. During the experiment, the developmental time, the adult stage's life duration, and the daily fecundity of each aphid were observed.

Life table and statistical analysis

The life table data of thiamethoxam-treated parental aphids (F0) and their offspring (F1) were evaluated using the age-stage, two-sex life table technique (Chi 1988; Chi et al. 2020, 2022b). The TWOSEX-MS Chart computer program (Chi et al. 2022a; Chi 2023a) was used to calculate the parameters such as the age-stage specific survival rate (sxj), the age-specific survival rate (lx), the age-stage reproductive value (vxj), as well as life history traits such as reproductive days, development time, male and female longevity, the adult pre-reproductive period (APOP), the total pre-reproductive period (TPOP), fecundity (F) (eggs/female), the intrinsic rate of increase (r), the finite rate of increase (λ), the net reproductive rate (R0), the mean generation time (T). To compute the differences and SEs, 100,000 bootstrap replicates were performed (Efron & Tibshirani 1993; Huang & Chi 2012; Akca et al. 2015; Akköprü et al. 2015). At a 5% significant level, the paired bootstrap test was used to evaluate the differences in demographic parameters between the thiamethoxam-exposed groups and the control group based on the confidence interval of the difference (Wei et al. 2020).

Population projection

The population projections for the control group and the cohorts treated with LC5 and LC10 of thiamethoxam were determined using the TIMING-MSChart program (Chi 2023b) following the methodology outlined by Chi (1990). In each cohort (control, LC5, and LC10), the initial aphid population consisted of ten newborn nymphs. These populations were projected over a period of 60 days under the assumption of no suppression by biotic or abiotic factors. To estimate the uncertainty of projection 100,000 bootstrap iterations were performed, and the resulting net reproductive rate (R0) values were sorted to determine the 2.5th and 97.5th percentiles, corresponding to the 2,500th and 97,500th sorted bootstrap samples. Subsequently, the bootstrap life table samples associated with the R0 values at the 2.5th and 97.5th percentiles were utilized to project the population for an additional 60 days. These results highlighted the variability and uncertainty inherent in the projected populations by illustrating confidence intervals (Huang et al. 2018).

Results

Toxicity of thiamethoxam on Aphis gossypii

The toxicity of thiamethoxam against adult cotton aphids was investigated using leaf-dip bioassay procedure. Results showed that thiamethoxam was highly toxic against adult A. gossypii after 48 h exposure with the LC50 value of 0.313 mg L−1 with confidence interval of 0.262–0.371 mg L−1 (Table 1). The LC5 and LC10 values of thiamethoxam against adult cotton aphids were 0.057 mg L−1 with confidence interval of 0.037–0.078 mg L−1 and 0.083 mg L−1 with confidence interval of 0.058–0.108 mg L−1 (Table 1). The sublethal concentrations (LC5 and LC10) were selected to investigate the direct effects of thiamethoxam on parental aphids and indirect effects (transgenerational) on the biological and demographic parameters of progeny generation A. gossypii.

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

The longevity and fecundity of A. gossypii adults were considerably impacted by the LC5 and LC10 of thiamethoxam (Table 2). The longevity of A. gossypii decreased extensively after exposure to the LC5 and LC10 of thiamethoxam, compared to the control (P < 0.05). The A. gossypii treated with LC5 and LC10 had a decreased fecundity compared to the untreated control (P < 0.05). The LC10 individuals treated with thiamethoxam had the lowest number of reproductive days than the LC5 and control group (Table 2, P < 0.05).

Table 2 Sublethal effects of thiamethoxam LC5 and LC10 on adult longevity, fecundity, and reproductive days of the F0 generation of Aphis gossypii
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Developmental duration and adult longevity of F1 Aphis gossypii

The transgenerational sublethal effects on F1 A. gossypii whose parents (F0) were exposed to the LC5 and LC10 of thiamethoxam are presented in Table 3. Results indicated a substantial reduction in the developmental period of the 1st instar when treated with thiamethoxam at LC5 and LC10 concentrations, as compared to the control group (Table 3, (P < 0.05). The developmental duration of 3rd instar A. gossypii was statistically shortened (P < 0.05) at LC5 concentration, while no effects were observed for the LC10 group compared to the control. The duration of 2nd and 4th instar aphids was not affected at both concentrations (P < 0.05). Consequently, when the parental aphids were exposed to the LC5 and LC10 of thiamethoxam, the pre-adult period of F1 A. gossypii was dramatically reduced compared to the control group (P < 0.05). Conversely, thiamethoxam considerably improved (P < 0.05) the adult longevity and total longevity of F1 aphids at the LC5 and LC10 compared to the control group (Table 3).

Table 3 Duration (days) of different developmental stages of Aphis gossypii F1 generation, originated from parents (F0) treated with LC5 and LC10 of thiamethoxam
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Reproduction and life table parameters of F1 Aphis gossypii

The reproductive and life table parameter effects of thiamethoxam on F1 aphids, whose parental generation was subjected to LC5 and LC10 concentrations (Table 4). These values displayed the transgenerational effect of the insecticide. Results demonstrated that the net reproductive rate (R0) and adult prereproductive period (APRP) of F1 aphids at the LC5 and LC10 concentrations have no significant difference (P < 0.05) compared to the control. The intrinsic rate of increase (r) and the finite rate of increase (λ) were significantly increased (P < 0.05) in the F1 generation at both LC5 and LC10 concentrations. Similarly, compared to control, the fecundity (F) and reproductive days (RPd) of F1 individuals were increased (P < 0.05) at both concentrations. However, the mean generation time (T) and total prereproductive period (TPRP) were substantially reduced (P < 0.05) at both the LC5 and LC10 of thiamethoxam as compared to the control group (Table 4).

Table 4 Reproduction and life table parameters of Aphis gossypii F1 generation, originated from parents (F0) treated with LC5 and LC10 of thiamethoxam
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The sxj represented the probability of a freshly born A. gossypii nymph surviving to age x and stage j (Fig. 1). The differences in the developing and adult stages of A. gossypii resulted in several overlaps between the LC5, LC10, and control groups. The lx, mx, and lxmx curves for the LC5, LC10, and control groups are shown in Fig. 2. The sublethal concentrations of thiamethoxam stimulated the lx, mx, and lxmx parameters of A. gossypii compared to the control. The exj indicates the predicted duration of an individual aphid of age x and stage j after age x (Fig. 3). The curves show that, in comparison to control, the F1 generation of A. gossypii is likely to survive longer in the LC5 and LC10 treatments of thiamethoxam. The vxj curves illustrate the population's adherence to potential offspring from age x to stage j (Fig. 4). The LC5 and LC10 treatments of thiamethoxam had elevated vxj values compared to the control.

Fig. 1
figure 1

Age-stage specific survival rate (sxj) of F1 generation Aphis gossypii originated from F0 individuals treated with the LC5 and LC10 of thiamethoxam

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Fig. 2
figure 2

Age-specific survival rate (lx), age-specific fecundity (mx), and the age-specific maternity (lxmx) of F1 generation Aphis gossypii originated from F0 individuals exposed with the LC5 and LC10 of thiamethoxam

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Fig. 3
figure 3

Age-stage life expectancy (exj) of progeny generation Aphis gossypii (F1) originated from parental aphids treated with the LC5 and LC10 of thiamethoxam

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Fig. 4
figure 4

Age-stage reproductive value (vxj) of progeny generation Aphis gossypii (F1) originated from parental aphids treated with the LC5 and LC10 of thiamethoxam

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Population projection

The population projections and their corresponding percentiles (2.5th and 97.5th) for the progeny generation (F1) of A. gossypii, whose parental generation was subjected to LC5 and LC10 concentrations of thiamethoxam for a 60-day period, are plotted in Fig. 5. Notably, the lowest total population size of A. gossypii was observed in the cohort derived from the untreated control group, comprising approximately 6.9 million individuals. Conversely, population projections for the F1 progeny exposed to LC5 and LC10 concentrations of thiamethoxam yielded nearly 24 million and 23 million individuals, respectively, thereby indicating clear hormesis effects in comparison to the control population. Significantly, the total population sizes of A. gossypii treated with LC5 and LC10 concentrations of thiamethoxam were markedly higher than those of the untreated control group after a 60-day period (Fig. 5).

Fig. 5
figure 5

Projected total population size (Nt) after 60 days for the progeny generation Aphis gossypii (F1) originated from parental aphids treated with the LC5 and LC10 of thiamethoxam and control group using the life table data from the original cohort and the cohorts generated by incorporating the 2.5 and 97.5% percentiles of R0 (net reproductive rate)

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Discussion

In the present work, we examined the transgenerational and sublethal effects of thiamethoxam (LC5 and LC10) on two successive generations (F0 and F1) of A. gossypii. Following a 48-h treatment period, the results revealed that thiamethoxam leaned more toxic to A. gossypii, with an LC50 of 0.313 mg/l. Aphids exposed to thiamethoxam exhibit transgenerational sublethal/hormesis effects on their biological parameters and lethal toxicity (Ullah et al. 2020). According to these findings, the LC5 and LC10 concentrations may be crucial for managing cotton aphids in field environments.

The current study demonstrates that after exposure to the sublethal concentrations of thiamethoxam for 48 h, the longevity and fecundity of adult A. gossypii (F0) were decreased. Our findings are consistent with (Ma et al. 2022), who reported that treatment with LC10 of afidopyropen dramatically decreased the lifespan and fecundity of paternal adult A. gossypii. Similarly, decreased fecundity and longevity of the cotton aphid were observed by (Ullah et al. 2019a) following direct exposure to the LC5 and LC15 of imidacloprid. The flupyradifurone was administered to M. persicae at sublethal concentrations, and the unfavorable effects, including a shorter lifespan and reduced fertility, were also noted (Tang et al. 2019). The greenbug, Schizaphis graminum (Rondani) (Hemiptera: Aphididae) was exposed to low lethal concentrations of acetamiprid, which drastically decreased its total longevity and fecundity (Vakhide & Safavi. 2014). As a result of sublethal concentrations of cycloxaprid being introduced to parental A. gossypii, Cui et al. (2018) also noted a decline in longevity and fertility. These results proved that sublethal concentrations of insecticides significantly affect the adult lifespan and fertility of the surviving aphids in addition to their lethal effects.

The parental aphids (F0), when exposed to the LC5 and LC10 of thiamethoxam, significantly impacted the developmental phases of F1 A. gossypii. Results showed that the developmental duration of 1st instar of F1 A. gossypii was significantly decreased at both concentrations while reduced only in LC5 of the 3rd instar of A. gossypii compared to the control. The parental generation (F0), when treated with the LC5 and LC10 of thiamethoxam, the pre-adult stage was considerably shorter in the offspring aphids (F1) compared to the control group. As opposed to the untreated aphids group, thiamethoxam markedly increased the adult longevity and total longevity of F1 aphids at both concentrations when F0 aphids were treated with LC5 and LC10. These results showed that after 48 h of exposure, the sublethal concentrations of thiamethoxam positively impacted the development and total lifespan of A. gossypii. (Ullah et al. 2019a) observed a reduction in the developmental duration of 4th instar and pre-adult stage of F1 A. gossypii when LC5 and LC15 concentrations of imidacloprid were applied to parental aphids (F0). The 3rd and 4th instars developmental duration of M. persicae, as well as the pre-adult stages, were considerably reduced after 48 h of exposure to the LC25 of flupyradifurone (Tang et al. 2019). Thiamethoxam at low lethal concentrations notably shortened the duration of the fourth instar in F1 A. gossypii (Ullah et al. 2020). The developmental time of A. gossypii (F1 generation) was dramatically shortened by sublethal doses of cycloxaprid, according to (Yuan et al. 2017). The adult longevity of the F1 generation of A. gossypii was greatly extended when the parental generation (F0) was subjected to sublethal and low lethal concentrations of thiamethoxam and imidacloprid (Ullah et al. 2019a, 2020). Tang et al. (2019) concluded that treating the parental aphids (F0) with the LC25 of flupyradifurone greatly increased the longevity of the F1 and F2 generations of M. persicae. The lifespan of both male and female Nilaparvata lugens (Stål) (Hemiptera: Delphacidae) exhibited a notable increase after being subjected to the LC20 concentration of nitenpyram for six consecutive generations (Gong et al. 2022).

In the current research, parental aphids exposed to the LC5 and LC10 of thiamethoxam cause transgenerational hormesis effects in A. gossypii compared to untreated aphids. The female fecundity (F) and reproductive days (RPd) were dramatically increased, while the mean generation time (T) and total pre-reproductive period (TPRP) were significantly reduced in the offspring generation (F1). Consequently, the demographic parameters, specifically the intrinsic rate of increase (r) and finite rate of increase (λ), were substantially higher in the LC5 and LC10 treatments than in the control. These alterations to the life history traits of A. gossypii showed that transgenerational hormetic effects evolved after parental aphids were exposed to the sublethal concentrations of thiamethoxam. Aphis gossypii exhibited this hormetic response without apparent fitness trade-offs following exposure to the LC5 and LC10 of thiamethoxam. The occurrence of simultaneous hormetic effects in various traits has been documented in A. gossypii when exposed to thiamethoxam, imidacloprid, and acetamiprid (Ullah et al. 2019a, 2019b, 2020) and M. persicae when subjected to flupyradifurone, acetamiprid, and imidacloprid (Ayyanath et al. 2013; Sial et al. 2018; Tang et al. 2019). The study conducted by (Gong et al. 2022) investigated the phenomenon of transgenerational hormesis in N. lugens following a six-generation exposure to LC20 nitenpyram for 96 h. The mean generation time and the pre-adult developmental duration of the N. lugens F-Sub6 strain were found to be drastically decreased in the LC20 of nitenpyram. In our current research, a similar phenomenon was observed; the pre-adult developmental length and mean generation time (T) of cotton aphids significantly declined in the LC5 and LC10 treated groups compared to the control. At 60 days post-exposure, the estimated A. gossypii population size in the thiamethoxam-treated groups was higher than in the control group. The results of this study indicate that insects exhibited increased adaptability to insecticide stress following exposure to hormetic concentrations of insecticide, which typically arise after degradation. Agricultural insect pests that are expected to experience numerous and successive low and sublethal stress levels may need to develop their hormesis (Rix et al. 2016; Cutler et al. 2022). Ullah et al. (2020) reported the hormetic effects of thiamethoxam on F1 individuals of A. gossypii, which might be due to the intermittent changes in expression of genes linked to fertility, growth and insecticide detoxification. The increased mRNA transcription level of the vitellogenin gene (Vg) might be translated into an increased reproduction of F1 generation following exposure of parental A. gossypii (F0) to the LC5 and LC15 of acetamiprid (Ullah et al. 2019b). However, future studies are needed to understand the in-depth underlying molecular mechanisms of transgenerational hormetic effects of insecticides on insects. In general, the findings of this study provide solid evidence that the sublethal concentrations of thiamethoxam induce transgenerational hormetic effects on the demographic parameters of A. gossypii. The implications of these findings are quite significant in terms of pest management through the use of insecticides.

Conclusion

The fecundity, lifespan, and reproductive days of the parental generation of A. gossypii were all considerably decreased following exposure to the sublethal concentrations of thiamethoxam. Furthermore, the LC5 and LC10 of thiamethoxam had transgenerational effects on the subsequent generation (F1) by altering the key demographic parameters. To the best of our knowledge, this is the first study to investigate the transgenerational hormetic effects of thiamethoxam on the biological parameters of cotton aphids. However, future research should explore the multi-generational hormesis effects of thiamethoxam on A. gossypii under field contexts.