Next Article in Journal
The Comparative Field Evaluation of Four Different Traps for Mosquito Surveillance in the Republic of Korea
Previous Article in Journal
Functional Morphology and Ultrastructure of the Peripheral Antennal Sensillar System of Graphosoma italicum (Müller, 1766) (Insecta: Hemiptera: Pentatomidae)
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Insects
Volume 15
Issue 7
10.3390/insects15070529
insects-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Intergenerational Sublethal Effects of Flonicamid on Cotton Aphid, Aphis gossypii: An Age-Stage, Two-Sex Life Table Study

by
Hina Gul
1,
Ali Güncan
2,
Farman Ullah
3,
Nicolas Desneux
4,* and
Xiaoxia Liu
1,*
1
MARA Key Laboratory of Pest Monitoring and Green Management, Department of Entomology, College of Plant Protection, China Agricultural University, Beijing 100193, China
2
Department of Plant Protection, Faculty of Agriculture, Ordu University, 52200 Ordu, Turkey
3
State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, China
4
Université Côte d’Azur, INRAE, CNRS, UMR ISA, 06000 Nice, France
*
Authors to whom correspondence should be addressed.
Insects 2024, 15(7), 529; https://doi.org/10.3390/insects15070529
Submission received: 10 June 2024 / Revised: 5 July 2024 / Accepted: 10 July 2024 / Published: 13 July 2024
(This article belongs to the Section Insect Pest and Vector Management)
Browse Figures
Versions Notes

Abstract

:

Simple Summary

Aphis gossypii Glover is an economically important sap-sucking insect pest that causes severe damage worldwide. The flonicamid has been widely used for controlling sap-sucking insect pests, but its intergenerational sublethal effects on key demographic parameters of A. gossypii have not been fully studied. The age-stage, two-sex life table analysis was conducted to investigate the sublethal effects of flonicamid on the biological parameters of adult A. gossypii (F0) and its subsequent intergenerational effects on the offspring (F1 generation). The results showed that the sublethal concentrations of flonicamid significantly decreased the longevity, fecundity, and reproductive days of F0 A. gossypii. Moreover, flonicamid induced intergenerational sublethal effects on the subsequent progeny generation (F1) by impacting the key biological and demographic parameters of A. gossypii. Taken together, these results demonstrated that sublethal concentrations of flonicamid negatively affect the demographic parameters of A. gossypii, resulting in the suppression of population growth.

Abstract

Flonicamid is a novel systemic insecticide widely used against aphids. However, the intergenerational sublethal effects of flonicamid on cotton aphid, Aphis gossypii, have not been fully studied. This study aimed to evaluate the sublethal effects of flonicamid on the biological parameters of adult A. gossypii (F0) and its subsequent intergenerational effects on the offspring (F1 generation) through age-stage, two-sex life table analysis. The results of the bioassays indicate that flonicamid exhibits significant toxicity toward adult A. gossypii, as evidenced by an LC50 value of 0.372 mg L−1 after a 48-h exposure period. The longevity, fecundity, and reproductive days of adult cotton aphids (F0) were significantly decreased when treated with the sublethal concentrations of flonicamid. The pre-adult stage exhibited an increase, whereas the adult longevity, total longevity, and fecundity experienced a notable decrease in F1 aphids after the exposure of F0 aphids to sublethal concentrations of flonicamid. Furthermore, the key demographic parameters, including r, λ, R0, and RPd, showed a significant decrease, while the total pre-reproductive period (TPRP) experienced a significant increase in the F1 generation. Collectively, our findings indicate that sublethal concentrations of flonicamid impact the demographic parameters of A. gossypii, resulting in suppression of population growth. This study presents comprehensive information on the overall impact of flonicamid on A. gossypii, which could potentially aid in managing this major pest.

1. Introduction

The cotton aphid, Aphis gossypii Glover (Hemiptera: Aphididae), is a serious sap-sucking insect pest that incurs substantial financial costs globally. Aphis gossypii inflicts severe agricultural damage through direct feeding, as well as indirect damage through virus transmission and honeydew contamination [1]. Several alternative pest management options are available [2,3,4,5], but insecticide application is still considered a major option in IPM [6,7]. Flonicamid is a recently developed systemic insecticide that poses a significant threat to sap-sucking insect pests [8,9,10]. Flonicamid exhibits high efficacy against phloem-feeding insects, including white flies, mealybugs, leafhoppers, thrips, jassids, scales, and aphids, by impeding their ability to engage in feeding behavior in the immediate aftermath of treatment [11]. Recently, Gul et al. (2023) reported that sublethal concentrations of flonicamid significantly affected key life-history traits on Schizaphis graminum (Rondani) (Hemiptera: Aphididae) [12]. The sublethal concentrations of flonicamid decreased the fecundity of Myzus persicae (Sulzer) (Hemiptera: Aphididae) [13]. The sublethal and low lethal concentrations of flonicamid significantly reduced the longevity and fecundity as well as the mRNA expression levels of genes related to the development and reproduction of A. gossypii [8]. Furthermore, Ren et al. (2018) revealed that sublethal concentrations of flonicamid inhibited the activity of Kir1 channels and influenced the secretion of honeydew and saliva in Nilaparvata lugens (Stål) (Hempitera: Delphacidae) [10].
Agroecosystems may subject insects to sublethal concentrations of chemical insecticides due to biotic or abiotic factors contributing to incorrect use or degradation [14,15]. Arthropods exposed to chemical insecticide residues experience sublethal effects [16,17]. Insects and their subsequent generations experience a direct impact on life-history parameters due to these sublethal effects [8,18,19,20]. The sublethal effects of insecticides are determined by several aspects, including dose/concentration [21,22]. The metabolic activities of exposed individuals are stimulated by insecticide doses and concentrations, which affect the insect growth parameters [23]. Hormesis phenomena refer to the occurrence of stimulation at low doses or concentrations and inhibition at higher doses or concentrations [24]. As a result, sublethal effects are essential to determine whether insecticides have an overall impact on target or non-target pests [25]. Insecticides have sublethal effects on the physiological and behavioral characteristics of the directly exposed insects, including feeding activity, lifespan, developmental period, and fertility, as opposed to their lethal effects [26,27,28,29]. These intergenerational sublethal effects influence subsequent generations, ultimately leading to community alterations and ecological services [30,31]. The age-stage, two-sex life table approach is widely used to investigate the life-history traits of insects after exposure to different biotic and abiotic constraints [32,33,34,35]. This approach has been broadly used for investigating the lethal, sublethal, and intergenerational effects of insecticides on insects [12,36,37].
In the current study, we aimed to determine the acute toxicity of flonicamid in adult A. gossypii. In addition, we used age-stage, two-sex life table analysis to investigate the sublethal effects of flonicamid on directly exposed F0 generation aphids and to assess its subsequent intergenerational effects on the F1 generation of A. gossypii. These findings provide in-depth knowledge about the overall impact of flonicamid on A. gossypii, which could help to control this major pest.

2. Material and Methods

2.1. Insect and Insecticide

The population of A. gossypii was collected from Xinjiang Uygur Autonomous Region of China in 1999 and was reared in the laboratory (22 ± 1 °C, 70 ± 10% R.H., 16:8 L:D) for more than 15 years without exposure to any insecticides. Insecticide-free fresh seedlings of the cotton plant, Gossypium hirsutum (L.) were used to rear A. gossypii. First, the seedlings were washed and put in plastic cups filled with water. The plastic cups were placed in a cage, and the aphids were carefully transferred with a soft brush. All experiments were conducted under laboratory conditions with 22 ± 1 °C, 70 ± 10% R.H, and 16:8 L:D.

2.2. Bioassays

Flonicamid toxicity against A. gossypii was determined by a previously described leaf-dipping approach [38] with slight modifications [18,39]. To evaluate the toxicity, the corresponding stock solution (highest concentration) was used to prepare six different concentrations of flonicamid. The cotton leaves were carefully divided into circular discs of 20 mm in diameter using a pointed steel punch. The cotton leaf discs were immersed in either flonicamid (2, 1, 0.5, 0.25, 0.125, and 0.0625 mg L−1) or distilled water (control) for 15 s. The treated leaf discs were placed on disposable polyethylene gloves at room temperature to dry naturally. The dried leaf discs were placed on 2% agar in 12-well cell plates. Adult A. gossypii (wingless) were transferred to leaf discs with a soft brush. The plates were covered with Chinese art paper, specifically Xuan paper, to prevent aphids from escaping. A minimum of 30 aphids were used in each replicate, and the procedure was replicated thrice for every concentration. The mortality rate was assessed 48 h after flonicamid exposure. The aphids were deemed dead if they exhibited immobility with gentle manipulation using a soft brush.

2.3. Sublethal Effects of Flonicamid on Life-History Traits of the F0 Generation

A total of 300 apterous adult cotton aphids were placed onto newly grown cotton plants. Adult aphids were taken out after 24 h, while the newly emerged nymphs were kept for further maturation into apterous adults. This approach ensures the same developmental stage of all aphids when first treated with the flonicamid and was considered as the F0 generation. Flonicamid was diluted with distilled water to make the LC5 (0.077 mg/L) and LC10 (0.109 mg/L) concentrations. Cotton leaf discs (20 mm) were subjected to a 15-s immersion in solutions containing different concentrations of flonicamid (LC5 and LC10), or in distilled water (control). Subsequently, each treated leaf disc was placed onto a plastic sheet and allowed to air at room temperature for drying. The desiccated leaf discs were transferred to agar within the 12-well cell-culture plates. The wingless adult aphids were then carefully transferred onto the cotton leaf discs and properly covered with filter paper to prevent any possibility of escape. The cell plates were placed within the incubator. After a 48-h duration, a total of 40 aphids that were still alive were individually relocated from each experimental group (LC5, LC10, and control) onto fresh cotton leaf discs measuring 20 mm in diameter without using insecticides. During the experiment, new insecticide-free cotton leaf discs were replaced every 2–3 days. The observation of development, survival, and fecundity was conducted daily. Nymphs that had just been born were counted daily and taken away until adult aphids died.

2.4. Intergenerational Effects of Flonicamid on the Biological Traits of F1 A. gossypii

The biological parameters of the progeny generation (F1) were investigated whose parents were subjected to LC5 and LC10 of flonicamid. The experimental procedure was performed on 40 newly born F1 offspring for the flonicamid treatments and the control group. Daily monitoring was conducted to determine the life table parameters such as development, fecundity, and longevity of the F1 aphids. After counting, the newly born nymphs were removed daily to ensure only adults remained in the cells. Insecticide-free cotton leaf discs were changed every two to three days until the adult aphids died. Developmental durations, longevity, and fecundity were assessed for each aphid throughout the experiment.

2.5. Statistical and Life Table Analysis

The bioassay data were analyzed by PoloPlus v2 (LeOra Software Inc., Berkeley, CA, USA). The life table data of all cohorts were analyzed using an age-stage, two-sex life table technique [33,40]. 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 like fecundity (F) (nymphs/female), reproductive days, adult longevity, development time, the adult pre-reproductive period (APRP), the total pre-reproductive period (TPRP), the intrinsic rate of increase (r), the finite rate of increase (λ), the net reproductive rate (R0), and the mean generation time (T) were assessed by a TWOSEX-MS Chart computer program [33,41]. The differences and standard errors (SEs) were investigated using 100,000 bootstrap replicates [42,43,44,45]. A paired bootstrap test (5% significant level) was used to assess the disparities in biological parameters between the flonicamid-exposed group and the control group on the basis of the confidence interval of the difference [46]. The detailed equations used for the life table analysis are shown in the Supplementary Materials File.

2.6. Population Projection

The population projections of different cohorts of A. gossypii were determined by the TIMING-MSChart program [47], according to the methodology described by [48]. The initial aphid population comprised ten newly born individuals in each cohort (control, LC5, and LC10). The populations were projected for 50 days, assuming no suppression by biotic or abiotic factors. To assess projection uncertainty, we conducted 100,000 bootstrap iterations and organized the resulting values of the net reproductive rate (R0). Then, the 2.5th and 97.5th percentiles, corresponding to the 2500th and 97,500th sorted bootstrap samples, were identified. The bootstrap life table samples were used to project the population for 50 days, resulting in these R0 values at the 2.5th and 97.5th percentiles. These findings underscored the uncertainty of the projected populations, obtaining confidence intervals of the projections [49].

3. Results

3.1. Toxicity of Flonicamid on Adult Aphis gossypii

The objective of this study was to assess the toxicity of flonicamid in adult cotton aphids using a leaf-dip bioassay procedure. The experimental findings indicated the high toxicity of flonicamid against adult A. gossypii following 48 h of treatment. The lethal concentrations that cause 50% mortality (LC50) were determined to be 0.372 mg L−1 (0.318–0.437 mg L−1) with slope ± SE of 2.403 ± 0.205 (χ2 = 8.826, df = 16, p = 0.920). The LC5 and LC10 values of flonicamid against adult cotton aphids were 0.077 mg L−1 (0.054–0.100 mg L−1), and 0.109 mg L−1 (0.081–0.136 mg L−1), respectively. The LC5 and LC10 were chosen to explore the direct effects of flonicamid on parental aphids as well as the indirect effects (intergenerational) on the biological and demographic parameters of progeny generation A. gossypii.

3.2. Sublethal Effects of Flonicamid on Parental Aphis gossypii (F0)

The adult longevity and fecundity of Aphis gossypii were significantly affected by the LC5 and LC10 of flonicamid (Table 1). A significant reduction in the longevity of A. gossypii was observed following exposure to flonicamid concentrations (LC5 and LC10), compared to the control group (p < 0.05). Adult cotton aphids subjected to LC5 and LC10 treatments exhibited a notable reduction in fecundity compared to the untreated control group (p < 0.05). The flonicamid-treated LC5 and LC10 individuals had fewer reproductive days than those in the control group (Table 1, p < 0.05).

3.3. Duration of Development and Adult Longevity of F1 Aphis gossypii

The intergenerational sublethal effects on F1 aphids whose parents were subjected to flonicamid LC5 and LC10 concentrations are presented in Table 2. The findings showed that exposure to flonicamid at LC10 concentration resulted in a slight prolongation of the developmental period of the 1st instar compared to the control group (Table 2, p < 0.05). However, there were no significant differences in the duration of 2nd and 3rd instar aphids at the LC5 and LC10 concentrations compared to the control (p < 0.05). The duration of the 4th instar and preadult period of A. gossypii increased statistically in the LC10 group, followed by the LC5 (p < 0.05). As a result, adult longevity and total longevity of F1 aphids decreased substantially at the LC5 and LC10 of flonicamid when the parental aphids were subjected to both concentrations compared to the control group (Table 2).

3.4. Reproduction and Life Table Parameters of F1 Aphis gossypii

The reproduction and life-history traits of progeny generation (F1) are shown in Table 3. The results demonstrated that R0, fecundity, and reproductive days (RPd) of F1 aphids were substantially decreased (p < 0.05) at the LC10 followed by the LC5 of flonicamid. The r and λ were substantially reduced at LC5 and LC10 concentrations. In contrast, there was no statistically significant difference (p < 0.05) observed in the APRP and T of F1 aphids at the LC5 and L C10 concentrations. However, the TPRP was significantly higher in both the LC5 and LC10 of flonicamid (p < 0.05) (Table 3).
The sxj curves show the probability of newly developed A. gossypii surviving to age x and stage j (Figure 1). The plotted curves of sxj clearly indicate that the sublethal concentrations of flonicamid significantly reduced developmental and adult stages. The impact of the lx, mx, and lxmx curves for the flonicamid and control groups of the cotton aphid is shown in Figure 2. The curves of lx, mx, and lxmx of A. gossypii were substantially affected in the sublethal concentrations of flonicamid as compared to the control (Figure 2). The exj curves represent the estimated duration of an individual (A. gossypii) at a specific age x and stage j, indicating the duration of survival beyond age x (Figure 3). The F1 A. gossypii lifespan is probably reduced after the parental generation (F0) is exposed to the LC5 and LC10 concentrations of flonicamid. The vxj highlights the affection of a population at age x and stage j towards their prospective progeny Figure 4). The lowest vxj values were reported in LC10, followed by LC5, of flonicamid.

3.5. Population Projection

Population projections (50 days) and confidence intervals (2.5th and 97.5th) for the F1 A. gossypii are shown in Figure 5. Notably, the cohort originating from the untreated control group exhibited the largest total population size of A. gossypii, exceeding one million individuals. In contrast, the projections for the F1 progeny whose parents were exposed to flonicamid at LC5 and LC10 concentrations indicated approximately 350 and 235 thousand aphids, respectively. The total population sizes of A. gossypii treated with flonicamid at LC5 and LC10 concentrations were lower than those of the untreated control group after 50 days (Figure 5).

4. Discussion

In the current study, we examined the intergenerational sublethal effects of flonicamid on two subsequent generations (F0 and F1) of A. gossypii. The 48 h bioassay results indicated the high toxicity of flonicamid against adult cotton aphids. Several studies reported that sublethal concentrations of pesticides significantly affect the physiological and behavioral traits of exposed insects [14,26,27,28,50]. Hence, it is essential to examine the intergenerational sublethal effects of flonicamid on the biological and demographic parameters of A. gossypii, which might be useful for controlling this major pest. The results of this study show that adult A. gossypii (F0) had reduced longevity and fecundity after being exposed to sublethal concentrations of flonicamid for 48 h.
Our results are in line with a previous study that the longevity and fecundity of F0 Schizaphis graminum (Rondani) were substantially reduced following exposure to the sublethal concentrations of flonicamid [12]. Similar reduced fecundity was observed by Shi et al. (2022) when they exposed A. gossypii to the sublethal and low lethal concentrations of flonicamid [8]. Afidopyropen at sublethal concentrations greatly reduced the longevity and fecundity of F0 A. gossypii [51]. Also, A. gossypii experienced a reduction in fecundity and longevity when directly exposed to the LC5 and LC15 of imidacloprid [18]. The negative consequences, such as a decreased fertility rate and a shorter lifespan, were observed in M. persicae, when subjected to the sublethal concentrations of flupyradifurone [52]. The overall lifespan and reproductive capabilities of S. graminum experienced a substantial drop when exposed to sublethal concentrations of acetamiprid [53]. Furthermore, Cui et al. (2018) observed a decrease in longevity and fertility in parental A. gossypii after treatment with sublethal concentrations of cycloxaprid [54]. These findings demonstrated that adult longevity and fecundity were negatively affected when insects survived after exposure to the insecticide residues.
The developmental stages of F1 A. gossypii were considerably affected by the exposure of the parental aphids (F0) to the sublethal concentrations of flonicamid. The results indicated increased preadult stages of F1 A. gossypii at sublethal concentrations of flonicamid. The flonicamid markedly decreased the adult longevity and total longevity of F1 aphids. These findings indicated that the developmental stages and overall lifespan of A. gossypii were adversely affected by sublethal concentrations of flonicamid. Shi et al. (2021) documented the prolonged developmental duration of 1st instar A. gossypii at sublethal and low lethal concentrations of flonicamid [8]. Recently, Gul et al. (2023) reported that the LC5 and LC10 of flonicamid significantly increased the preadult stages while reducing the adult longevity of S. graminum [12]. The increased preadult stages and shorter longevity of F1 A. gossypii were noted at sublethal concentrations of afidopyropen [51]. Extended developmental durations of F1 A. gossypii were also reported for thiamethoxam and methyl benzoate treatments [19,55]. However, several studies have documented a reduction in the developmental durations of F1 individuals when the F0 was treated with insecticides [19,52,56]. The F1 A. gossypii had decreased longevity when the F0 generation was exposed to clothianidin, flupyradifurone, and buprofezin [16,57,58]. Buprofezin and abamectin at low lethal concentrations affect the longevity of Sogatella furcifera Horváth (Hemiptera: Delphacidae) and Scolothrips longicornis Priesner (Thysanoptera: Thripidae) [59,60]. Prolonged developmental stages and reduced longevity did not indicate the hormetic effects of flonicamid on progeny aphids (F1) after exposure of F0 individuals to sublethal concentrations. This trade-off occurs when insects allocate energy towards detoxifying chemical pesticides, enabling their survival but at the expense of their development [61,62,63,64].
The key demographic traits of F1 aphids significantly decreased at sublethal concentrations of flonicamid, suggesting that flonicamid may have potential value as an insecticide even at sublethal concentrations. Significantly decreased biological traits such as R0, r, λ, and fecundity were observed in the F1 A. gossypii, while the TPRP was substantially prolonged compared to the control. Similar decreased key demographic parameters such as fecundity, R0, r, and λ were noted when S. graminum were exposed to sublethal concentrations of flonicamid [50]. Ma et al. (2022) reported that the fecundity, r, and λ, were significantly decreased at the LC10 of afidopyropen [51]. Sulfoxaflor, imidacloprid, and clothianidin negatively affected the biological traits of S. graminum following treatment with sublethal and low lethal concentrations [65]. Koo et al. (2015) reported reduced R0, longevity, and fecundity in A. gossypii at low lethal concentrations of flonicamid [66]. The LC25 of sulfoxaflor dramatically reduced the population growth of A. gossypii [67]. Reduced fecundity in A. gossypii was observed when treated with sublethal concentrations of spirotetramat [68]. Yuan et al. (2017) also showed similar results in which LC10 of cycloxaprid resulted in a notable decrease in the lifespan and reproductive capabilities of F0 and F1 generation aphids [56]. Non-lethal insecticide-induced adverse effects on the life history parameters of individuals could potentially influence population growth [69]. The current study showed that flonicamid, even at sublethal concentrations, affects the directly exposed individuals and the progeny generations owing to intergenerational sublethal effects, which ultimately impact the population growth of A. gossypii.

5. Conclusions

In general, the current study demonstrated that sublethal concentrations of flonicamid significantly decreased the life-history traits of F0 A. gossypii. Moreover, we reported that flonicamid induces intergenerational sublethal effects on the F1 by impacting the biological and demographic parameters of A. gossypii. The obtained results have the potential to be valuable in the development of control strategies for A. gossypii. However, additional research is necessary to figure out the long-term sublethal effects of flonicamid on multiple generations under field conditions.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/insects15070529/s1, References [70,71,72,73] are cited in the supplementary materials.

Author Contributions

Conceptualization, methodology, and writing—original draft preparation: H.G., F.U., N.D., and X.L.; visualization, investigation, and validation: A.G., H.G., and F.U.; resources: X.L.; data curation and analysis: A.G., and H.G.; Writing—reviewing and editing: A.G., H.G., and F.U.; supervision and project administration: X.L., and N.D. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the National Key R&D Program of China (2022YFD1400300).

Data Availability Statement

All data analyzed during this study are included in this published article.

Conflicts of Interest

The authors have no relevant financial or non-financial interests to disclose.

References

  1. Hullé, M.; Chaubet, B.; Turpeau, E.; Simon, J. Encyclop’Aphid: A website on aphids and their natural enemies. Entomol. Gen. 2020, 40, 97–101. [Google Scholar] [CrossRef]
  2. Verheggen, F.; Barrès, B.; Bonafos, R.; Desneux, N.; Escobar-Gutiérrez, A.J.; Gachet, E.; Laville, J.; Siegwart, M.; Thiéry, D.; Jactel, H. Producing sugar beets without neonicotinoids: An evaluation of alternatives for the management of viruses-transmitting aphids. Entomol. Gen. 2022, 42, 491–498. [Google Scholar] [CrossRef]
  3. Zang, L.-S.; Wang, S.; Zhang, F.; Desneux, N. Biological control with Trichogramma in China: History, present status and perspectives. Annu. Rev. Entomol. 2021, 66, 463–484. [Google Scholar] [CrossRef] [PubMed]
  4. Monticelli, L.S.; Desneux, N.; Biondi, A.; Mohl, E.; Heimpel, G.E. Post-introduction changes of host specificity traits in the aphid parasitoid Lysiphlebus testaceipes. Entomol. Gen. 2022, 42, 559–569. [Google Scholar] [CrossRef]
  5. Gao, X.; Xue, H.; Zhu, X.; Wang, L.; Zhang, K.; Li, D.; Ji, J.; Liang, J.; Luo, J.; Cui, J. Parasitism by Lysiphlebia japonica alters the microbiome of Aphis gossypii offspring. Entomol. Gen. 2023, 43, 1071–1075. [Google Scholar] [CrossRef]
  6. Abbas, A.; Zhao, C.R.; Arshad, M.; Han, X.; Iftikhar, A.; Hafeez, F.; Aslam, A.; Ullah, F. Sublethal effects of spinetoram and emamectin benzoate on key demographic parameters of fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae) under laboratory conditions. Environ. Sci. Pollut. Res. 2023, 30, 82990–83003. [Google Scholar] [CrossRef]
  7. Dai, H.; Tian, L.; Sun, X.; Wang, X.; Zhu, X.; Monticelli, L.S.; Ullah, F.; Zhao, J.; Desneux, N.; Wang, S. Spirotetramat-and thiamethoxam-induced sublethal effects increase spread of tomato chlorosis virus by its vector Bemisia tabaci. Entomol. Gen. 2023, 43, 1051–1059. [Google Scholar] [CrossRef]
  8. Shi, D.; Luo, C.; Lv, H.; Zhang, L.; Desneux, N.; You, H.; Li, J.; Ullah, F.; Ma, K. Impact of sublethal and low lethal concentrations of flonicamid on key biological traits and population growth associated genes in melon aphid, Aphis gossypii Glover. Crop Prot. 2022, 152, 105863. [Google Scholar] [CrossRef]
  9. Roditakis, E.; Fytrou, N.; Staurakaki, M.; Vontas, J.; Tsagkarakou, A. Activity of flonicamid on the sweet potato whitely Bemisia tabaci (Homoptera: Aleyrodidae) and its natural enemies. Pest Manag. Sci. 2014, 70, 1460–1467. [Google Scholar] [CrossRef]
  10. Ren, M.; Niu, J.; Hu, B.; Wei, Q.; Zheng, C.; Tian, X.; Gao, C.; He, B.; Dong, K.; Su, J. Block of Kir channels by flonicamid disrupts salivary and renal excretion of insect pests. Insect Biochem. Mol. Biol. 2018, 99, 17–26. [Google Scholar] [CrossRef]
  11. Kodandaram, M.; Rai, A.; Halder, J. Novel insecticides for management of insect pests in vegetable crops: A review. Veg. Sci 2010, 37, 109–123. [Google Scholar]
  12. Gul, H.; ul Haq, I.; Ullah, F.; Khan, S.; Yaseen, A.; Shah, S.H.; Tariq, K.; Güncan, A.; Desneux, N.; Liu, X. Impact of sublethal concentrations of flonicamid on key demographic parameters and feeding behavior of Schizaphis graminum. Ecotoxicology 2023, 32, 756–767. [Google Scholar] [CrossRef]
  13. Cho, S.-R.; Koo, H.-N.; Yoon, C.; Kim, G.-H. Sublethal effects of flonicamid and thiamethoxam on green peach aphid, Myzus persicae and feeding behavior analysis. J. Korean Soc. Appl. Biol. Chem. 2011, 54, 889–898. [Google Scholar] [CrossRef]
  14. Desneux, N.; Fauvergue, X.; Dechaume-Moncharmont, F.-X.; Kerhoas, L.; Ballanger, Y.; Kaiser, L. Diaeretiella rapae limits Myzus persicae populations after applications of deltamethrin in oilseed rape. J. Econ. Entomol. 2005, 98, 9–17. [Google Scholar] [CrossRef]
  15. Desneux, N.; Decourtye, A.; Delpuech, J.-M. The sublethal effects of pesticides on beneficial arthropods. Annu. Rev. Entomol. 2007, 52, 81–106. [Google Scholar] [CrossRef]
  16. Ullah, F.; Gul, H.; Desneux, N.; Tariq, K.; Ali, A.; Gao, X.; Song, D. Clothianidin-induced sublethal effects and expression changes of vitellogenin and ecdysone receptors genes in the melon aphid, Aphis gossypii. Entomol. Gen. 2019, 39, 137–149. [Google Scholar] [CrossRef]
  17. Gul, H.; Ullah, F.; Hafeez, M.; Tariq, K.; Desneux, N.; Gao, X.; Song, D. Sublethal concentrations of clothianidin affect fecundity and key demographic parameters of the chive maggot, Bradysia odoriphaga. Ecotoxicology 2021, 30, 1150–1160. [Google Scholar] [CrossRef]
  18. Ullah, F.; Gul, H.; Desneux, N.; Gao, X.; Song, D. Imidacloprid-induced hormesis effects on demographic traits of the melon aphid, Aphis gossypii. Entomol. Gen. 2019, 39, 325–337. [Google Scholar] [CrossRef]
  19. Ullah, F.; Gul, H.; Tariq, K.; Desneux, N.; Gao, X.; Song, D. Thiamethoxam induces transgenerational hormesis effects and alteration of genes expression in Aphis gossypii. Pestic. Biochem. Physiol. 2020, 165, 104557. [Google Scholar] [CrossRef]
  20. Jia, Z.Q.; Zhan, E.L.; Zhang, S.G.; Wang, Y.; Song, P.P.; Jones, A.K.; Han, Z.J.; Zhao, C.Q. Broflanilide prolongs the development of fall armyworm Spodoptera frugiperda by regulating biosynthesis of juvenile hormone. Entomol. Gen. 2022, 42, 61. [Google Scholar] [CrossRef]
  21. Cutler, G.C. Insects, insecticides and hormesis: Evidence and considerations for study. Dose-Response 2013, 11. [Google Scholar] [CrossRef]
  22. Decourtye, A.; Henry, M.; Desneux, N. Overhaul pesticide testing on bees. Nature 2013, 497, 188. [Google Scholar] [CrossRef] [PubMed]
  23. Rix, R.R.; Cutler, G.C. Review of molecular and biochemical responses during stress induced stimulation and hormesis in insects. Sci. Total Environ. 2022, 827, 154085. [Google Scholar] [CrossRef] [PubMed]
  24. Cutler, G.C.; Amichot, M.; Benelli, G.; Guedes, R.N.C.; Qu, Y.; Rix, R.R.; Ullah, F.; Desneux, N. Hormesis and insects: Effects and interactions in agroecosystems. Sci. Total Environ. 2022, 825, 153899. [Google Scholar] [CrossRef]
  25. Guedes, R.; Smagghe, G.; Stark, J.; Desneux, N. Pesticide-induced stress in arthropod pests for optimized integrated pest management programs. Annu. Rev. Entomol. 2016, 61, 43–62. [Google Scholar] [CrossRef] [PubMed]
  26. Ullah, F.; Gul, H.; Desneux, N.; Qu, Y.; Xiao, X.; Khattak, A.M.; Gao, X.; Song, D. Acetamiprid-induced hormetic effects and vitellogenin gene (Vg) expression in the melon aphid, Aphis gossypii. Entomol. Gen. 2019, 39, 259–270. [Google Scholar] [CrossRef]
  27. Aeinehchi, P.; Naseri, B.; Rafiee Dastjerdi, H.; Nouri-Ganbalani, G.; Golizadeh, A. Lethal and sublethal effects of thiacloprid on Schizaphis graminum (Rondani) (Hemiptera: Aphididae) and its predator Hippodamia variegata (Goeze) (Coleoptera: Coccinellidae). Toxin Rev. 2021, 40, 1261–1271. [Google Scholar] [CrossRef]
  28. Hafeez, M.; Ullah, F.; Khan, M.M.; Wang, Z.; Gul, H.; Li, X.; Huang, J.; Siddiqui, J.A.; Qasim, M.; Wang, R.-L. Comparative low lethal effects of three insecticides on demographical traits and enzyme activity of the Spodoptera exigua (Hübner). Environ. Sci. Pollut. Res. 2022, 29, 60198–60211. [Google Scholar] [CrossRef]
  29. Ullah, F.; Güncan, A.; Gul, H.; Hafeez, M.; Zhou, S.; Wang, Y.; Zhang, Z.; Huang, J.; Ghramh, H.A.; Guo, W.; et al. Spinosad-induced intergenerational sublethal effects on Tuta absoluta: Biological traits and related genes expressions. Entomol. Gen. 2024, 44, 395–404. [Google Scholar] [CrossRef]
  30. Lu, Y.; Wu, K.; Jiang, Y.; Guo, Y.; Desneux, N. Widespread adoption of Bt cotton and insecticide decrease promotes biocontrol services. Nature 2012, 487, 362. [Google Scholar] [CrossRef]
  31. Abd Allah, A.; Desneux, N.; Monticelli, L.S.; Fan, Y.; Shi, X.; Guedes, R.N.; Gao, X. Potential for insecticide-mediated shift in ecological dominance between two competing aphid species. Chemosphere 2019, 226, 651–658. [Google Scholar]
  32. Chi, H.; You, M.; Atlıhan, R.; Smith, C.L.; Kavousi, A.; Özgökçe, M.S.; Güncan, A.; Tuan, S.-J.; Fu, J.-W.; Xu, Y.-Y. Age-Stage, two-sex life table: An introduction to theory, data analysis, and application. Entomol. Gen. 2020, 40, 102–123. [Google Scholar] [CrossRef]
  33. Chi, H.; Güncan, A.; Kavousi, A.; Gharakhani, G.; Atlihan, R.; Özgökçe, M.S.; Shirazi, J.; Amir-Maafi, M.; Maroufpoor, M.; Taghizadeh, R. TWOSEX-MSChart: The key tool for life table research and education. Entomol. Gen. 2022, 42, 845–849. [Google Scholar] [CrossRef]
  34. Chi, H.; Kavousi, A.; Gharekhani, G.; Atlihan, R.; Özgökçe, M.S.; Güncan, A.; Gökçe, A.; Smith, C.L.; Benelli, G.; Guedes, R.N.C. Advances in theory, data analysis, and application of the age-stage, two-sex life table for demographic research, biological control, and pest management. Entomol. Gen. 2023, 43, 705–735. [Google Scholar] [CrossRef]
  35. Chi, H.; Kara, H.; Özgökçe, M.S.; Atlihan, R.; Güncan, A.; Rişvanlı, M.R. Innovative application of set theory, Cartesian product, and multinomial theorem in demographic research. Entomol. Gen. 2022, 42, 863–874. [Google Scholar] [CrossRef]
  36. Liu, X.; Fu, Z.; Zhu, Y.; Gao, X.; Liu, T.-X.; Liang, P. Sublethal and transgenerational effects of afidopyropen on biological traits of the green peach aphid Myzus persicae (Sluzer). Pestic. Biochem. Physiol. 2022, 180, 104981. [Google Scholar] [CrossRef]
  37. Ju, D.; Liu, Y.-X.; Liu, X.; Dewer, Y.; Mota-Sanchez, D.; Yang, X.-Q. Exposure to lambda-cyhalothrin and abamectin drives sublethal and transgenerational effects on the development and reproduction of Cydia pomonella. Ecotoxicol. Environ. Saf. 2023, 252, 114581. [Google Scholar] [CrossRef]
  38. Moores, G.D.; Gao, X.; Denholm, I.; Devonshire, A.L. Characterisation of insensitive acetylcholinesterase in insecticide-resistant cotton aphids, Aphis gossypii glover (homoptera: Aphididae). Pestic. Biochem. Physiol. 1996, 56, 102–110. [Google Scholar] [CrossRef]
  39. Gul, H.; Güncan, A.; Ullah, F.; Ning, X.; Desneux, N.; Liu, X. Sublethal concentrations of thiamethoxam induce transgenerational hormesis in cotton aphid, Aphis gossypii Glover. CABI Agric. Biosci. 2023, 4, 50. [Google Scholar] [CrossRef]
  40. Chi, H. Life-table analysis incorporating both sexes and variable development rates among individuals. Environ. Entomol. 1988, 17, 26–34. [Google Scholar] [CrossRef]
  41. Chi, H. TWOSEX-MS Chart: A Computer Program for the Age-Stage, Two-Sex Life Table Analysis. 2023. Available online: http://140.120.197.173/ecology/prod02.htm (accessed on 22 November 2023).
  42. Akca, I.; Ayvaz, T.; Yazici, E.; Smith, C.L.; Chi, H. Demography and population projection of Aphis fabae (Hemiptera: Aphididae): With additional comments on life table research criteria. J. Econ. Entomol. 2015, 108, 1466–1478. [Google Scholar] [CrossRef]
  43. Efron, B.; Tibshirani, R. An Introduction to the Bootstrap; Chapman and Hall Inc.: New York, NY, USA, 1993; Volune 914. [Google Scholar]
  44. Huang, Y.B.; Chi, H. Age-stage, two-sex life tables of Bactrocera cucurbitae (Coquillett) (Diptera: Tephritidae) with a discussion on the problem of applying female age-specific life tables to insect populations. Insect Sci. 2012, 19, 263–273. [Google Scholar] [CrossRef]
  45. Akköprü, E.P.; Atlıhan, R.; Okut, H.; Chi, H. Demographic assessment of plant cultivar resistance to insect pests: A case study of the dusky-veined walnut aphid (Hemiptera: Callaphididae) on five walnut cultivars. J. Econ. Entomol. 2015, 108, 378–387. [Google Scholar] [CrossRef] [PubMed]
  46. Wei, M.; Chi, H.; Guo, Y.; Li, X.; Zhao, L.; Ma, R. Demography of Cacopsylla chinensis (Hemiptera: Psyllidae) reared on four cultivars of Pyrus bretschneideri (Rosales: Rosaceae) and P. communis pears with estimations of confidence intervals of specific life table statistics. J. Econ. Entomol. 2020, 113, 2343–2353. [Google Scholar] [CrossRef]
  47. Chi, H. TIMING-MSChart: A Computer Program for the Population Projection Based on Age-Stage, Two-Sex Life Table; National Chung Hsing University: Taichung, Taiwan, 2023; Available online: http://140.120.197.173/ecology/prod02.htm (accessed on 28 November 2023).
  48. Chi, H. Timing of control based on the stage structure of pest populations: A simulation approach. J. Econ. Entomol. 1990, 83, 1143–1150. [Google Scholar] [CrossRef]
  49. Huang, H.-W.; Chi, H.; Smith, C.L. Linking demography and consumption of Henosepilachna vigintioctopunctata (Coleoptera: Coccinellidae) fed on Solanum photeinocarpum (Solanales: Solanaceae): With a new method to project the uncertainty of population growth and consumption. J. Econ. Entomol. 2018, 111, 1–9. [Google Scholar] [CrossRef]
  50. Gul, H.; Haq, I.U.; Güncan, A.; Abbas, A.; Khan, S.; Yaseen, A.; Ullah, F.; Desneux, N.; Liu, X. Thiamethoxam-Induced Intergenerational Sublethal Effects on the Life History and Feeding Behavior of Rhopalosiphum padi. Plants 2024, 13, 865. [Google Scholar] [CrossRef]
  51. Ma, K.-S.; Tang, Q.-L.; Liang, P.-Z.; Li, J.-H.; Gao, X.-W. A sublethal concentration of afidopyropen suppresses the population growth of the cotton aphid, Aphis gossypii Glover (Hemiptera: Aphididae). J. Integr. Agric. 2022, 21, 2055–2064. [Google Scholar] [CrossRef]
  52. Tang, Q.; Ma, K.; Chi, H.; Hou, Y.; Gao, X. Transgenerational hormetic effects of sublethal dose of flupyradifurone on the green peach aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae). PLoS ONE 2019, 14, e0208058. [Google Scholar] [CrossRef]
  53. Vakhide, N.; Safavi, S.A. Lethal and sublethal effects of direct exposure to acetamiprid on reproduction and survival of the greenbug, Schizaphis graminum (Hemiptera: Aphididae). Arch. Phytopathol. Plant Prot. 2014, 47, 339–348. [Google Scholar] [CrossRef]
  54. Cui, L.; Yuan, H.; Wang, Q.; Wang, Q.; Rui, C. Sublethal effects of the novel cis-nitromethylene neonicotinoid cycloxaprid on the cotton aphid Aphis gossypii Glover (Hemiptera: Aphididae). Sci. Rep. 2018, 8, 8915. [Google Scholar] [CrossRef] [PubMed]
  55. Mostafiz, M.M.; Alam, M.B.; Chi, H.; Hassan, E.; Shim, J.-K.; Lee, K.-Y. Effects of sublethal doses of methyl benzoate on the life history traits and acetylcholinesterase (AChE) activity of Aphis gossypii. Agronomy 2020, 10, 1313. [Google Scholar] [CrossRef]
  56. Yuan, H.B.; Li, J.H.; Liu, Y.Q.; Cui, L.; Lu, Y.H.; Xu, X.Y.; Li, Z.; Wu, K.M.; Desneux, N. Lethal, sublethal and transgenerational effects of the novel chiral neonicotinoid pesticide cycloxaprid on demographic and behavioral traits of Aphis gossypii (Hemiptera: Aphididae). Insect Sci. 2017, 24, 743–752. [Google Scholar] [CrossRef] [PubMed]
  57. Ullah, F.; Gul, H.; Yousaf, H.K.; Xiu, W.; Qian, D.; Gao, X.; Tariq, K.; Han, P.; Desneux, N.; Song, D. Impact of low lethal concentrations of buprofezin on biological traits and expression profile of chitin synthase 1 gene (CHS1) in melon aphid, Aphis gossypii. Sci. Rep. 2019, 9, 12291. [Google Scholar] [CrossRef] [PubMed]
  58. Liang, P.-Z.; Ma, K.-S.; Chen, X.-W.; Tang, C.-Y.; Xia, J.; Chi, H.; Gao, X.-W. Toxicity and Sublethal Effects of Flupyradifurone, a Novel Butenolide Insecticide, on the Development and Fecundity of Aphis gossypii (Hemiptera: Aphididae). J. Econ. Entomol. 2018, 112, 852–858. [Google Scholar] [CrossRef]
  59. Ali, E.; Liao, X.; Yang, P.; Mao, K.; Zhang, X.; Shakeel, M.; Salim, A.M.; Wan, H.; Li, J. Sublethal effects of buprofezin on development and reproduction in the white-backed planthopper, Sogatella furcifera (Hemiptera: Delphacidae). Sci. Rep. 2017, 7, 16913. [Google Scholar] [CrossRef] [PubMed]
  60. Pakyari, H.; Enkegaard, A. Sublethal and transgenerational effects of abamectin on the biological performance of the predatory thrips Scolothrips longicornis (Thysanoptera: Thripidae). J. Econ. Entomol. 2015, 108, 559–565. [Google Scholar] [CrossRef]
  61. Jager, T.; Barsi, A.; Ducrot, V. Hormesis on life-history traits: Is there such thing as a free lunch? Ecotoxicology 2013, 22, 263–270. [Google Scholar] [CrossRef]
  62. Guo, R.; Ren, X.; Ren, H. Effects of dimethoate on rotifer Brachionus calyciflorus using multigeneration toxicity tests. J. Environ. Sci. Health Part B 2012, 47, 883–890. [Google Scholar] [CrossRef]
  63. Hannig, G.T.; Ziegler, M.; Marçon, P.G. Feeding cessation effects of chlorantraniliprole, a new anthranilic diamide insecticide, in comparison with several insecticides in distinct chemical classes and mode-of-action groups. Pest Manag. Sci. Former. Pestic. Sci. 2009, 65, 969–974. [Google Scholar] [CrossRef]
  64. Mallqui, K.V.; Vieira, J.; Guedes, R.; Gontijo, L. Azadirachtin-induced hormesis mediating shift in fecundity-longevity trade-off in the Mexican bean weevil (Chrysomelidae: Bruchinae). J. Econ. Entomol. 2014, 107, 860–866. [Google Scholar] [CrossRef] [PubMed]
  65. Atta, B.; Rizwan, M.; Sabir, A.M.; Gogi, M.D.; Farooq, M.A.; Jamal, A. Lethal and sublethal effects of clothianidin, imidacloprid and sulfoxaflor on the wheat aphid, Schizaphis graminum (Hemiptera: Aphididae) and its coccinellid predator, Coccinella septempunctata. Int. J. Trop. Insect Sci. 2021, 41, 345–358. [Google Scholar] [CrossRef]
  66. Koo, H.N.; Lee, S.W.; Yun, S.H.; Kim, H.K.; Kim, G.H. Feeding response of the cotton aphid, Aphis gossypii, to sublethal rates of flonicamid and imidacloprid. Entomol. Exp. Appl. 2015, 154, 110–119. [Google Scholar] [CrossRef]
  67. Chen, X.; Ma, K.; Li, F.; Liang, P.; Liu, Y.; Guo, T.; Song, D.; Desneux, N.; Gao, X. Sublethal and transgenerational effects of sulfoxaflor on the biological traits of the cotton aphid, Aphis gossypii Glover (Hemiptera: Aphididae). Ecotoxicology 2016, 25, 1841–1848. [Google Scholar] [CrossRef] [PubMed]
  68. Gong, Y.; Shi, X.; Desneux, N.; Gao, X. Effects of spirotetramat treatments on fecundity and carboxylesterase expression of Aphis gossypii Glover. Ecotoxicology 2016, 25, 655–663. [Google Scholar] [CrossRef] [PubMed]
  69. Stark, J.D.; Banks, J.E. Population-level effects of pesticides and other toxicants on arthropods. Annu. Rev. Entomol. 2003, 48, 505–519. [Google Scholar] [CrossRef] [PubMed]
  70. Chen, G.-M.; Chi, H.; Wang, R.-C.; Wang, Y.-P.; Xu, Y.-Y.; Li, X.-D.; Yin, P.; Zheng, F.-Q. Demography and uncertainty of population growth of Conogethes punctiferalis (Lepidoptera: Crambidae) reared on five host plants with discussion on some life history statistics. J. Econ. Entomol. 2018, 111, 2143–2152. [Google Scholar] [CrossRef] [PubMed]
  71. Goodman, D. Optimal life histories, optimal notation, and the value of reproductive value. Am. Nat. 1982, 119, 803–823. [Google Scholar] [CrossRef]
  72. Chi, H.; Su, H.-Y. 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. [Google Scholar] [CrossRef]
  73. Tuan, S.J.; Lee, C.C.; Chi, H. Population and damage projection of Spodoptera litura (F.) on peanuts (Arachis hypogaea L.) under different conditions using the age-stage, two-sex life table. Pest Manag. Sci. 2014, 70, 805–813. [Google Scholar] [CrossRef]
Insects 15 00529 g001
Figure 1. Age-stage-specific survival rate (sxj) of F1 Aphis gossypii descended from the F0 aphids treated with LC5 and LC10 of flonicamid and control.
Figure 1. Age-stage-specific survival rate (sxj) of F1 Aphis gossypii descended from the F0 aphids treated with LC5 and LC10 of flonicamid and control.
Insects 15 00529 g001
Insects 15 00529 g002
Figure 2. Age-specific survival rate (lx), age-specific fecundity (mx), and the age-specific maternity (lxmx) of the F1 Aphis gossypii descended from the F0 aphids treated with LC5 and LC10 of flonicamid and control.
Figure 2. Age-specific survival rate (lx), age-specific fecundity (mx), and the age-specific maternity (lxmx) of the F1 Aphis gossypii descended from the F0 aphids treated with LC5 and LC10 of flonicamid and control.
Insects 15 00529 g002
Insects 15 00529 g003
Figure 3. Age-stage life expectancy (exj) of F1 Aphis gossypii descended from the F0 aphids treated with LC5 and LC10 of flonicamid and control.
Figure 3. Age-stage life expectancy (exj) of F1 Aphis gossypii descended from the F0 aphids treated with LC5 and LC10 of flonicamid and control.
Insects 15 00529 g003
Insects 15 00529 g004
Figure 4. Age-stage reproductive value (vxj) of F1 Aphis gossypii descended from the F0 aphids treated with LC5 and LC10 of flonicamid and control.
Figure 4. Age-stage reproductive value (vxj) of F1 Aphis gossypii descended from the F0 aphids treated with LC5 and LC10 of flonicamid and control.
Insects 15 00529 g004
Insects 15 00529 g005
Figure 5. Total population size (N(t)) for F1 Aphis gossypii descended from the F0 aphids treated with LC5 and LC10 of flonicamid and control (after 50 days) projected from the life table data using the original cohort and the generated cohorts by incorporating the 2.5 and 97.5% percentiles of R0.
Figure 5. Total population size (N(t)) for F1 Aphis gossypii descended from the F0 aphids treated with LC5 and LC10 of flonicamid and control (after 50 days) projected from the life table data using the original cohort and the generated cohorts by incorporating the 2.5 and 97.5% percentiles of R0.
Insects 15 00529 g005
Table 1. Impact of sublethal concentrations of flonicamid on the F0 generation of Aphis gossypii.
Table 1. Impact of sublethal concentrations of flonicamid on the F0 generation of Aphis gossypii.
ParametersControlFlonicamid (LC5)Flonicamid (LC10)
Mean ± SEMean ± SEMean ± SE
Adult longevity (days)22.80 ± 0.22 a19.30 ± 0.20 b15.80 ± 0.20 c
Fecundity (nymphs/female)35.10 ± 0.60 a26.40 ± 0.34 b21.70 ± 0.38 c
Reproductive days (days)21.50 ± 0.27 a17.03 ± 0.23 b14.05 ± 0.20 c
The means within a row followed by different lowercase letters indicate significant differences among the treatments.
Table 2. Effect of sublethal concentrations of flonicamid on the development of F1 Aphis gossypii descended from F0 generations.
Table 2. Effect of sublethal concentrations of flonicamid on the development of F1 Aphis gossypii descended from F0 generations.
Stage Control Flonicamid (LC5) Flonicamid (LC10)
nMean ± SEnMean ± SEnMean ± SE
First-instar nymph402.10 ± 0.10 b402.30 ± 0.08 ab402.40 ± 0.10 a
Second-instar nymph381.50 ± 0.09 a381.61 ± 0.08 a401.70 ± 0.09 a
Third-instar nymph381.61 ± 0.10 a371.51 ± 0.09 a391.62 ± 0.09 a
Fourth-instar nymph381.21 ± 0.07 c371.81 ± 0.10 b382.11 ± 0.10 a
Pre-adult386.45 ± 0.08 c377.24 ± 0.07 b387.71 ± 0.18 a
Adult (Female)3823.50 ± 0.27 a3720.62 ± 0.19 b3817.42 ± 0.20 c
Total longevity (Female)3829.95 ± 0.30 a3727.86 ± 0.19 b3825.13 ± 0.26 c
The means within a row followed by different lowercase letters indicate significant differences among the treatments (Paired bootstrap test, p < 0.05).
Table 3. Population parameters of F1 Aphis gossypii descended from the F0 generation exposed to flonicamid.
Table 3. Population parameters of F1 Aphis gossypii descended from the F0 generation exposed to flonicamid.
Parameters aControlFlonicamid (LC5)Flonicamid (LC10)
Mean ± SEMean ± SEMean ± SE
R0 (offspring/individual)33.08 ± 1.32 a26.83 ± 1.33 b22.63 ± 0.91 c
r (day−1)0.2494 ± 0.0044 a0.2281 ± 0.0045 b0.2194 ± 0.0050 b
λ (day−1)1.2832 ± 0.0057 a1.2562 ± 0.0057 b1.2453 ± 0.0062 b
T (days)14.03 ± 0.16 a14.42 ± 0.14 a14.22 ± 0.25 a
F (nymphs/female)34.82 ± 0.59 a29.00 ± 0.61 b23.82 ± 0.41 c
RPd (days)22.05 ± 0.30 a18.65 ± 0.21 b16.00 ± 0.25 c
APRP (days)0.13 ± 0.05 a0.19 ± 0.07 a0.11 ± 0.05 a
TPRP (days)6.58 ± 0.09 b7.43 ± 0.10 a7.82 ± 0.17 a
The means within a row followed by different lowercase letters indicate significant differences among the treatments (Paired bootstrap test, p < 0.05). a R0 = net reproductive rate; r = intrinsic rate of increase; λ = finite rate of increase; T = mean generation time; F = fecundity; RPd = reproductive days; APRP = adult prereproductive period; TPRP = total prereproductive period.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Gul, H.; Güncan, A.; Ullah, F.; Desneux, N.; Liu, X. Intergenerational Sublethal Effects of Flonicamid on Cotton Aphid, Aphis gossypii: An Age-Stage, Two-Sex Life Table Study. Insects 2024, 15, 529. https://doi.org/10.3390/insects15070529

AMA Style

Gul H, Güncan A, Ullah F, Desneux N, Liu X. Intergenerational Sublethal Effects of Flonicamid on Cotton Aphid, Aphis gossypii: An Age-Stage, Two-Sex Life Table Study. Insects. 2024; 15(7):529. https://doi.org/10.3390/insects15070529

Chicago/Turabian Style

Gul, Hina, Ali Güncan, Farman Ullah, Nicolas Desneux, and Xiaoxia Liu. 2024. "Intergenerational Sublethal Effects of Flonicamid on Cotton Aphid, Aphis gossypii: An Age-Stage, Two-Sex Life Table Study" Insects 15, no. 7: 529. https://doi.org/10.3390/insects15070529

APA Style

Gul, H., Güncan, A., Ullah, F., Desneux, N., & Liu, X. (2024). Intergenerational Sublethal Effects of Flonicamid on Cotton Aphid, Aphis gossypii: An Age-Stage, Two-Sex Life Table Study. Insects, 15(7), 529. https://doi.org/10.3390/insects15070529

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop