Next Article in Journal
Growth Performance, Waste Reduction Efficiency and Nutritional Composition of Black Soldier Fly (Hermetia illucens) Larvae and Prepupae Reared on Coconut Endosperm and Soybean Curd Residue with or without Supplementation
Previous Article in Journal
Using Matching Traits to Study the Impacts of Land-Use Intensification on Plant–Pollinator Interactions in European Grasslands: A Review
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Insects
Volume 12
Issue 8
10.3390/insects12080681
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

Transgenerational Effects of a Neonicotinoid and a Novel Sulfoximine Insecticide on the Harlequin Ladybird

by
Changchun Dai
1,2,3,
Michele Ricupero
4,
Zequn Wang
2,
Nicolas Desneux
5,
Antonio Biondi
4 and
Yanhui Lu
1,*
1
State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China
2
Department of Plant Protection, College of Agriculture, Northeast Agricultural University, Harbin 150030, China
3
Langfang Experimental Station of the Chinese Academy of Agricultural Sciences, Langfang 065005, China
4
Department of Agriculture Food and Environment, University of Catania, 95123 Catania, Italy
5
Université Côte d’Azur, INRAE, CNRS, UMR ISA, 06000 Nice, France
*
Author to whom correspondence should be addressed.
Insects 2021, 12(8), 681; https://doi.org/10.3390/insects12080681
Submission received: 16 June 2021 / Revised: 24 July 2021 / Accepted: 26 July 2021 / Published: 28 July 2021
Browse Figure
Versions Notes

Abstract

:

Simple Summary

The coccinellid Harmonia axyridis is an important natural enemy of various agricultural pests, including aphids. Agrochemicals can negatively affect the performance of arthropod natural enemies and, thus, the ecological services they provide. In this context, we assessed the lethal and sublethal effects of two neuroactive compounds with different chemical structures: the long-established neonicotinoid insecticide, imidacloprid, and the novel, sulfoximine insecticide, sulfoxaflor, both of which act on nicotinic acetylcholine receptors against adult and developmental stages of H. axyridis. Estimated LC20 and LC50 doses of imidacloprid for a target pest species, Aphis gossypii, resulted in significantly greater mortality in contact bioassays against adult H. axyridis compared with equivalent LC20 and LC50 doses of sulfoxaflor. Both concentrations of imidacloprid and sulfoxaflor significantly reduced the proportion of ovipositing females of parental generation. LC20 and LC50 dose of imidacloprid and LC50 dose of sulfoxaflor significantly reduced both the fecundity and fertility of parental generation. In progeny of parents exposed to both insecticides at LC50 concentrations the juvenile survival rate was significantly reduced, and both concentrations of imidacloprid and sulfoxaflor, except LC20 dose of sulfoxaflor, significantly prolonged the larval development time. These experimental results disclose the negative influence of sulfoxaflor and imidacloprid at low concentrations on the harlequin ladybird and its subsequent generation. Hence, actions should be taken to optimize imidacloprid and sulfoxaflor applications for the control of aphid pests, aiming at preserving the biocontrol services provided by this important predator.

Abstract

The harlequin ladybird, Harmonia axyridis Pallas (Coleoptera: Coccinellidae), is a generalist predator and an effective biocontrol agent of various insect pests that has been exploited for the control of aphid pests in the greenhouse and field. However, insecticides are widely used to control aphid pests worldwide and the potential non-target effects of sulfoxaflor and imidacloprid for controlling aphid pests towards this biocontrol agent are little known. Although both sulfoxaflor and imidacloprid act on nicotinic acetylcholine receptors of insects, sulfoxaflor has a novel chemical structure compared with neonicotinoids. We assessed the lethal, sublethal and transgenerational effects of sulfoxaflor and imidacloprid on H. axyridis simultaneously exposed via ingestion of contaminated prey and via residual contact on the host plant at LC20 and LC50 doses estimated for the cotton aphid. Imidacloprid significantly reduced the survival of H. axyridis adults compared to sulfoxaflor at the same lethal concentration against cotton aphid. Both concentrations of imidacloprid and sulfoxaflor reduced the proportion of ovipositing females, and both concentrations of imidacloprid and sulfoxaflor, except LC20 dose of sulfoxaflor, reduced the fecundity and fertility of the parental generation. In the progeny of imidacloprid- and sulfoxaflor-exposed parents, both tested LC50 concentrations significantly decreased the juvenile survival rate, and both concentrations of imidacloprid and sulfoxaflor, except LC20 dose of sulfoxaflor, prolonged the development time. Our findings provide evidence of the negative influence of imidacloprid and sulfoxaflor at low lethal concentrations on the harlequin ladybird and on the progeny of exposed individuals, i.e., transgenerational effects. Hence, these findings stress the importance of optimizing the applications of imidacloprid and sulfoxaflor for the control of aphid pests, aiming at preserving the biocontrol services provided by H. axyridis throughout the integrated pest management approach.

1. Introduction

The harlequin ladybird, Harmonia axyridis Pallas (Coleoptera: Coccinellidae), is native to Asia, and since the last century it has been introduced into Europe and North America as a biological control agent against aphids and coccids [1,2,3]. Harmonia axyridis represents a key biological control agent for a variety of plant pests, with a broad dietary range and great capacity to suppress plant pests in both natural and agroecosystems [4,5,6,7]. For example, in cotton, abundant H. axyridis predators can suppress aphid populations below the economic threshold at seedling stages [8,9,10].
The cotton aphid, Aphis gossypii Glover (Hemiptera: Aphididae), a key pest of cotton, causes serious damage to cotton yield by sucking sap and transmitting viruses [11,12,13]. Although integrated pest management (IPM) programs have been implemented against A. gossypii, its management still primarily depends on the application of insecticides [14,15,16,17]. As a consequence, the overuse of pesticides can cause increasing resistance of primary pests, outbreaks of secondary pests and disruption of the ecosystem functioning and services for beneficial arthropods [18,19,20,21]. In China, A. gossypii has been controlled with neonicotinoids and more recently sulfoxamines in the past few years [18,22].
Over the last decades, imidacloprid has been used worldwide to control sap-sucking pests [23,24,25,26], and its use has increased significantly. However, long-term and extensive application of imidacloprid has led to increasing resistance of cotton aphids to imidacloprid [25,27]. Resistance to imidacloprid has been attributed in some cases to increased rates of insecticide detoxification or to mutations in nicotinic acetylcholine receptor (nAChR) [28,29]. Sulfoxaflor, a sulfoximine insecticide, has a proved efficacy for controlling a variety of sap-sucking pests and a recognized low toxicity towards mammals [30,31,32,33,34]. Although the actions of sulfoxaflor and imidacloprid were characterized at nAChRs of insect, sulfoxaflor has a limited cross-resistance towards neonicotinoid resistant pests due to its novel chemical structure [31,35,36]. For this reason, and the widespread occurrence of cotton aphid resistance to imidacloprid, sulfoxaflor is being increasingly used for the control of resistant cotton aphids [37]. By contrast, imidacloprid is suspected to lead to the disruption of ecological services and environmental pollution [38]. A plethora of studies in unison recognized the negative impact of neonicotinoid insecticides on natural enemies and pollinators even at low doses [39,40,41,42,43,44,45]. As a consequence, three neonicotinoid insecticides (i.e., imidacloprid, clothianidin and thiamethoxam) were recently banned for outdoor application in Europe in 2019 [46].
The evaluation of non-target effects of insecticides on beneficial arthropods generally includes both lethal and sublethal effects [39]. The former studies the acute toxicity and gives immediate feedback on the direct mortality caused by the pesticide [47]. The latter considers the physiological and behavioral impairments caused by the chemical to the non-target organisms, which may induce the reduction of their ecological services [48]. Coccinellid predators can be exposed to pesticides by direct contact with spray droplets and/or foliar residues of neonicotinoid insecticide when they are foraging on the crop, as well as by consuming the contaminated diet when feeding on food (e.g., pollen, prey) in the field [18,49,50,51,52,53,54]. Thus, the effects of pesticides at low dose/concentration on natural enemies frequently occurs after pesticide applications in the field [55,56,57,58].
To the best of our knowledge, several studies on acute toxicity of imidacloprid and sulfoxaflor to non-target natural enemies such as ladybeetle predators have been conducted [49,59]. However, the potential long-term influence of imidacloprid and sulfoxaflor on H. axyridis has been scarcely investigated [59]. Hence, we have explored the transgenerational impact of low lethal concentrations of sulfoxaflor and imidacloprid on H. axyridis. The results are expected to provide a valuable reference for optimizing the use of sulfoxaflor and imidacloprid as an effective component of IPM programs in agricultural settings.

2. Materials and Methods

2.1. Biological Materials

Aphis gossypii and H. axyridis laboratory colonies were originally obtained from infested cotton plants collected in cotton fields at the Langfang Experimental Station of the Chinese Academy of Agricultural Sciences (CAAS), Hebei Province, China, during summer in 2017.
The cotton aphid was continuously reared in screened cages (50 cm × 50 cm × 50 cm) on cotton plants (cv. “Zhongmian49”) in the laboratory at 24 ± 2 °C, 50 ± 10% RH, and L16:D8 photoperiod. The colony of A. gossypii was maintained in the laboratory for more than twenty generations before being used in the experiments. Cotton plants were grown in plastic pots (13 cm high, 15 cm diameter) with standard potting soil and then enclosed in cages without pesticides treatment during the plant growth period. Cotton plants at the five-leaf stage were used for cotton aphid rearing as well as for all the experiments.
Individuals of H. axyridis were reared on Megoura japonica Matsumura (Hemiptera: Aphididae), which were fed on pesticide-free seedlings of broad beans, Vicia faba L., at 20 ± 2 °C, 50 ± 10% RH, and L12:D12 photoperiod. The aphid-infested seedings of broad beans were offered to H. axyridis every two days within a fine mesh net plastic cage. Broad beans were cultivated in plastic pots. The laboratory conditions were the same as described above for the rearing of A. gossypii.

2.2. Chemicals

Commercial formulations of sulfoxaflor and imidacloprid commonly used for the control of cotton aphid were first tested to evaluate the baseline toxicity against A. gossypii laboratory colony. The concentrations causing the 20% (LC20) and 50% (LC50) mortality of A. gossypii were estimated (see Section 2.3), and these concentrations were then used to assess the lethal and sublethal effects on H. axyridis. Full information on the pesticides used in this experiment is summarized in Table 1. All tested pesticides were supplied by manufacturers in China.

2.3. Insecticide Baseline Toxicity on Prey

The dipping method [60] was used for assessing the concentration-mortality response of sulfoxaflor and imidacloprid on A. gossypii. Six serial concentrations of each insecticide formulation (3.50 ppm, 7.00 ppm, 14.00 ppm, 35.00 ppm, 70.00 ppm and 140.00 ppm for imidacloprid; 2.20 ppm, 5.50 ppm, 11.00 ppm, 22.00 ppm, 55.00 ppm and 110.00 ppm for sulfoxaflor) were diluted with distilled water for the bioassay. To obtain coetaneous A. gossypii young adults, 3-day-old nymphs of A. gossypii were collected from the rearing cage and moved to clean and uninfested cotton plants with a fine paint brush. After 7 days, excised cotton leaves bearing 20 coetaneous (24–48 h old) young adults A. gossypii were immersed in one of six pesticide solutions for 5 s and then were allowed to dry in laboratory conditions for 1 h. The control group was treated with distilled water. Each insecticide-concentration and the control were replicated five times, and cotton leaves per treatment with 20 young adults of A. gossypii were placed in individual Petri dishes (contain agar plate), which were covered with perforated PVC film. These Petri dishes were kept for 48 h in climatic chambers. A. gossypii mortality was scored by counting the number of surviving individuals under a stereomicroscope after the beginning of the exposure. The individuals were recorded as dead when they failed to crawl when pushed with a fine brush.
All the experiments were carried out under controlled environmental conditions at 25 ± 1 °C, 70 ± 5% RH, L16:D8 photoperiod and light intensity of 24,000 Lx in climatic chambers (RXZ-500D, Jiangnan Instrument Factory, Ningbo, China).

2.4. Lethal Toxicity on Harmonia Axyridis

We estimated the acute toxicity of LC20 and LC50 doses of imidacloprid and sulfoxaflor against H. axyridis adults by simulating a field exposure. Because H. axyridis in the field can be simultaneously exposed to insecticide residues through contact and ingestion, respectively, on contaminated-plants and contaminated-prey, we used the methodology proposed by Dai et al. [61]. Briefly, young and unmated H. axyridis females (60–72 h old) from the rearing were exposed for three days to insecticide residues of the chosen insecticides at their LC50 and LC20 on aphid infested cotton plants. Through preliminary observations, twelve pots infested by mixed cotton aphid colonies (more than 2000 aphids per pot) were considered optimal to satisfy for three days the feeding uptake of 20 H. axyridis females. Aphid infested cotton pots were sprayed by the insecticidal solutions within a distance of 0.5 m with a 2 L hand sprayer until the solution ran off leaves, and they were left to dry for 1 h in laboratory conditions. Per each replicate, 20 H. axyridis young unmated females were exposed to fresh insecticide residues on treated infested cotton plants for 3 days inside a ventilated and screened with fine mesh net. The mortality of H. axyridis was recorded after 72 h of exposure. Harmonia axyridis individuals were considered dead when they did not react after being touched with a fine brush. Control treatment consisted of untreated infested plants sprayed by distilled water. Five replicates were carried out per each insecticide-concentration and the control.

2.5. Sublethal Effect on Longevity and Reproductive Traits

The sublethal impact of the imidacloprid and sulfoxaflor at their LC20 and LC50 doses, previously calculated for the target pest, was assessed on the longevity, fecundity and fertility of the surviving females from the bioassay “2.3 Lethal toxicity on Harmonia axyridis”. Each surviving female was paired with an untreated male of the same age. Each pair of female and male H. axyridis was transferred with a fine brush to a ventilated Petri dish (9 cm diameter, 2 cm high) and fed with sterilized Ephestia kuehniella Zeller (Lepidoptera: Pyralidae) eggs, since this factitious prey has been recognized as an optimal food source for the laboratory rearing of H. axyridis [62]. The E. kuehniella eggs were provided daily, the Petri dishes were cleaned daily, and water was offered to the adults for all the treatments. A Z-fold filter paper was also fixed into each Petri dish as an artificial oviposition substrate. Oviposition and egg hatching for each female were recorded for 30 days from the first egg-laying event, while longevity was measured for females until they died. A representative 10% of each fresh egg batch was picked out and isolated in one hole of a 24-hole plate and checked daily to assess the hatch rate until 50 eggs per couple were tested. Between 72 and 139 adult couples were studied per each pesticide-concentration and the control.

2.6. Transgenerational Effects on Offspring Survival Rate and Developmental Time

The fresh eggs (≤12 h) of the first batch laid by H. axyridis females exposed to insecticide in “2.3 Lethal Toxicity on H. Axyridis” were individually transferred with a wet soft fine brush into a ventilated Petri dish (3.5 cm diameter, 1.5 cm high) for hatching (2–3 eggs per couple). New hatchlings were fed with E. kuehniella eggs daily, and Petri dishes were cleaned daily. For all treatments, water was supplied through a soaked cotton wad in the Petri dish, and cotton was replaced daily.
The development parameters of larvae were recorded every 24 h. A total of 150 newly hatched larvae were reared per each insecticide-concentration and for the untreated control.

2.7. Statistical Analysis

The LC20 and LC50 values for imidacloprid and sulfoxaflor were estimated by Probit analysis [63] after 48 h exposure to insecticides. The concentration–mortality relationships were considered true when the observed data and the estimated data did not significantly differ (p < 0.05).
Levene and Shapiro–Wilk tests were used to check the homogeneity and normality of variance of the dataset that was transformed whenever required. The effects of the two insecticides (factor: insecticide), their LCs (factor: concentration) and their interaction (insecticide x concentration) on the mortality of female adults were analyzed by factorial ANOVA. The longevity of females to different insecticide-concentration exposure was analyzed using the Kaplan–Meier procedure followed by the log rank (Mantel–Cox) test among treatments. The reproductive parameters were analyzed using the ANOVA for the fecundity and fertility data. Differences among the insecticide treatments in the ANOVAs were highlighted by Tukey’s HSD test. Developmental duration of offspring and survival rate of juveniles of H. axyridis were analyzed by Kaplan–Meier estimate. Statistical analyses were carried out on SPSS Statistics v. 20.0 (IBM Corp., Armonk, NY, USA).

3. Results

3.1. Insecticide Baseline Toxicity on Prey

From the log-probit regression analysis, the LC20 and LC50 values of imidacloprid and sulfoxaflor to A. gossypii adults were estimated and listed in Table 2. Observed data fit the log-probit model and no statistically significant deviation from the regression equation was observed. Imidacloprid exhibited the highest toxicity against the cotton aphid laboratory population showing lower LCs values in comparison to sulfoxaflor insecticide (Table 2).

3.2. Lethal Toxicity on Harmonia Axyridis

The mortality of the females of H. axyridis exposed simultaneously to dry residues by contact on sprayed plants and by ingestion of contaminated prey after 3 days was significantly affected by the insecticides (at the LC20 of insecticides, F2,12 = 60.041, p < 0.001; at the LC50 of insecticides, F2,12 = 205.682, p < 0.001), the concentration of LC20 and LC50 (imidacloprid, F2,12 = 119.465, p < 0.001; sulfoxaflor, F2,12 = 103.258, p < 0.001) and their interaction (F5,24 = 136.693, p < 0.001) (Figure 1). Both insecticides and concentrations caused a significantly higher mortality of the exposed predators compared to the control. Namely, LC50s of the two insecticides caused significantly higher mortality than LC20s. Compared to mortality caused by sulfoxaflor at LC50 (31.20 ± 1.50%), imidacloprid at LC50 (55.20 ± 2.33%) was the most harmful insecticide to H. axyridis females. In the LC20 experiment, the result was similar with the LC50 experiment, that is, imidacloprid with a mean mortality of 33.60 ± 2.71% caused a higher lethal effect than sulfoxaflor with an average mortality of 18.40 ± 1.60%.

3.3. Influence of Insecticides on Longevity and Fecundity of Females

Statistically significant differences were found in the longevity (χ2 = 12.139, df = 4, p = 0.016) of females between the insecticide-concentration combination and control. Moreover, sulfoxaflor LC20 significantly increased longevity of female adults. The adult longevity of other treatments showed no significant differences with control treatment; however, imidacloprid at LC50 significantly decreased longevity of female adults compare with LC20 and LC50 doses of sulfoxaflor.
Low lethal concentrations of sulfoxaflor and imidacloprid significantly reduced the percentage of females able to lay eggs. The influence of sulfoxaflor on female fertility rate (χ2 = 52.217, df = 4, p < 0.001) at the same sublethal concentration was less than that of imidacloprid, but there were no statistically significant differences between them. Meanwhile, the fecundity per female was significantly reduced to all sublethal concentrations (F4,342 = 5.670, p < 0.001) except for sulfoxaflor LC20 in comparison to the control (Table 3).

3.4. Effect of Insecticides on Survival Rate and Developmental Time of Offspring

The effect of the LC20 and LC50 concentrations of imidacloprid and sulfoxaflor on egg hatchability, larval survival and adult emergence of F1 generation are presented in Table 4. The egg hatchability (F4,342 = 8.254, p < 0.001) of H. axyridis significantly decreased at LC50s of imidacloprid and sulfoxaflor compared to the control; however, LC20 of imidacloprid and sulfoxaflor showed no significant differences with control. No significant differences were found between imidacloprid and sulfoxaflor at the same sublethal concentration. The sublethal concentration of imidacloprid and sulfoxaflor significantly affected the survival of H. axyridis larvae (overall comparisons, χ2 = 19.104, df = 4, p = 0.001). In Harmonia axyridis larvae, F1 generation of female parents exposed to imidacloprid LC50 led to the lowest survivorship, while sulfoxaflor LC20 induced the highest survivorship. According to analysis of pupal survival (χ2 = 8.248, df = 4, p = 0.083), the sublethal concentration of two insecticides led to a decrease in pupal survival in comparison to control, but no significant differences were found between the two insecticides and the two concentrations.
The influence of imidacloprid and sulfoxaflor at the two low lethal concentrations on developmental time of the F1 generation (egg, larva and pupa) of H. axyridis is listed in Table 5. LC20 of sulfoxaflor caused no significant impact on the developmental time of egg (χ2 = 75.812, df = 4, p < 0.001) and larva (χ2 = 102.805, df = 4, p < 0.001), and other insecticide treatments significantly lengthened the developmental time of egg and larva in comparison to control treatment. No significant differences were found in the pupal developmental time (χ2 = 16.703, df = 4, p = 0.002) between the treatments and control, but sulfoxaflor at LC50 significantly prolonged the developmental time of pupa compared to LC20.
Imidacloprid and sulfoxaflor at the LC20 and LC50 doses significantly lengthened developmental time (1st instar, χ2 = 38.055, df = 4, p < 0.001; 2nd instar, χ2 = 24.727, df = 4, p < 0.001; 3rd instar, χ2 = 64.632, df = 4, p < 0.001; 4th instar, χ2 = 76.762, df = 4, p < 0.001) of instars, especially for the 1st, 3rd and 4th instars (Table 6).

4. Discussion

The present study provides evidence of acute and sub-lethal effects of imidacloprid and sulfoxaflor against adults female H. axyridis. Transgenerational sub-lethal effects of these insecticides were also found in the progeny of surviving females mated with untreated males.
Dai et al. reported that imidacloprid (0.503 ppm, 3.186 ppm) and sulfoxaflor (0.397 ppm, 2.000 ppm) have no significant lethal effect on female H. axyridis [61]. Here the results on acute toxicity are not in accordance with Dai et al. [61], because LC20 and LC50 values are higher in the present study. Such differences in toxicity toward the target pest may be due to the different susceptibility of the A. gossypii strains used in the various experiments, with the population of the present study being less susceptible to the two chemicals compared to the other study.
In our study, the results showed no significant effect of imidacloprid with LC20 and LC50 concentrations and sulfoxaflor with LC50 concentrations on the longevity of H. axyridis females. However, sublethal concentration (LC20) of sulfoxaflor significantly increased longevity of H. axyridis. This was probably because the sulfoxaflor was very safe at LC20 concentration, and the number of spawned eggs of sulfoxaflor (LC20) treatment were less than the control. H. axyridis, treated by sulfoxaflor (LC20), can spend more energy to maintain non-reproductive life activities. Skouras et al. reported that imidacloprid at sublethal concentrations reduced longevity of Hippodamia variegata (Coleoptera: Coccinellidae) [64]. Papachristos et al. reported a similar result, which demonstrated that low concentration of imidacloprid can reduce longevity of Hippodamia undecimnotata (Coleoptera: Coccinellidae) [65]. However, in agreement with our findings, Rahmani et al. reported that sublethal concentrations of thiamethoxam had no significant negative effect on longevity of H. variegate when the 3rd instar larvae were exposed [66]. The results of insecticide effects on longevity of ladybird beetles were variable, which may be influenced by the molecular structure of the insecticide and the treatment method.
Sublethal concentrations (LC20 and LC50) of imidacloprid and sulfoxaflor had significant negative influences on adult fecundity and egg hatchability of H. axyridis when the 3-day-old females were exposed. These results are in accordance with Jiang et al., Yu et al. and Xiao et al. [67,68,69]. Jiang et al. reported that thiamethoxam at LC10 and 0.1 × LC10 had significant negative effects on survival rate, adult emergence rate, fecundity and egg hatchability of Coccinella septempunctata L. (Coleoptera: Coccinellidae). Yu et al. reported that imidacloprid, at sublethal concentrations, might impair adult emergence and reproduction of C. septempunctata. Xiao et al. found sublethal effects on the reproduction of C. septempunctata residually exposed to 10% of LC5 and LC5 of imidacloprid.
The sublethal and transgenerational effects of insecticides have been overlooked in many cases, even though they may negatively affect beneficial arthropod communities and have a significant impact on ecological services [39,48,70,71]. Moreover, we evaluated the transgenerational effects of imidacloprid and sulfoxaflor on survival rate and developmental time of H. axyridis. Our results demonstrated that the rates of hatching, larvae survival and emergence significantly decreased, and the egg and instar stages of the F1 generation could apparently be prolonged, when its parental generation F0 were exposed to imidacloprid and sulfoxaflor at the LC20 and LC50 concentrations. Xiao et al. found that the progeny of these individuals of C. septempunctata had a lower demographical growth compared to the untreated control (transgenerational effects) [69]. Similarly, thiamethoxam applied to cotton seed influenced larvae or adults of Chrysoperla externa and H. axyridis, which also reduced juvenile survival of individuals in the following generation [72].
Overall, the present study disclosed that low concentrations of sulfoxaflor and imidacloprid can cause acute toxicity and impair the biological parameters of a parental generation of H. axyridis and its offspring by contact on plant and ingestion of contaminated prey. However, sulfoxaflor caused lower mortality and affected less H. axyridis biological traits at intra- and transgenerational levels than imidacloprid, thus proving to be a safer compound in the laboratory. Nonetheless, further specific long-term studies are necessary to reveal the mechanisms behind the effect of low insecticide concentrations on H. axyridis.
Our outcomes stress also the need to include in-depth biological evaluations into pesticide risk-assessment schemes towards beneficial arthropods. Numerous studies recognized the importance of addressing studies on pesticide sublethal effect [73,74]. Similarly, the combination of chemical stressors with different thermal regimes can be assessed towards beneficial predators considering the ever-changing environment as projected by the current global warming scenario [75].

5. Conclusions

Experimental results indicated that low concentrations of sulfoxaflor and imidacloprid both had acute toxicity against H. axyridis and negative sublethal effects on its population development. Therefore, sulfoxaflor and imidacloprid should be cautiously used in IPM programs against A. gossypii. Otherwise, the ecological service and effectiveness of harlequin ladybirds will be reduced. Compared with the traditional nicotinic insecticide imidacloprid, sulfoxaflor appears safer for the harlequin ladybird, which has less influence on the survival rate of ladybird adults and progeny and their fecundity. The results of this study will further improve our understanding of the effects of insecticide residues on ladybird population development and provide a basis for more scientific and efficient measures to manage A. gossypii and protect coccinellid beetles.

Author Contributions

Conceptualization, Y.L., A.B.; methodology, C.D., M.R.; investigation, C.D. and Z.W.; data analysis, Y.L. and C.D.; writing—original draft preparation, C.D.; writing—review and editing Y.L., A.B., N.D. and M.R.; visualization, Y.L., C.D., A.B. and M.R.; Funding Acquisition, Y.L. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the National Natural Science Funds of China (U2003212), and China Agriculture Research System (CARS-15-19).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available on request from the corresponding authors.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Koch, R.L. The multicolored Asian lady beetle, Harmonia axyridis: A review of its biology, uses in biological control, and non-target impacts. J. Pest Sci. 2003, 1, 32. [Google Scholar] [CrossRef] [Green Version]
  2. Brown, P.M.J.; Adriaens, T.; Bathon, H.; Cuppen, J.; Goldarazena, A.; Hägg, T.; Kenis, M.; Klausnitzer, B.E.M.; Kovář, I.; Loomans, A.J.M.; et al. Harmonia axyridis in Europe: Spread and distribution of a non-native coccinellid. BioControl 2008, 53, 5–21. [Google Scholar] [CrossRef] [Green Version]
  3. Roy, H.E.; Brown, P.M.; Adriaens, T.; Berkvens, N.; Borges, I.; Clusella-Trullas, S.; Comont, R.F.; Clercq, P.D.; Eschen, R.; Estoup, A.; et al. The harlequin ladybird, Harmonia axyridis: Global perspectives on invasion history and ecology. Biol. Invasions 2016, 18, 997–1044. [Google Scholar] [CrossRef]
  4. Hodek, I.; Honek, A.; Van Emden, H.F. Ecology and Behaviour of the Ladybird Beetles (Coccinellidae); John Wiley &Sons: Hoboken, NJ, USA, 2012. [Google Scholar]
  5. Riddick, E.W. Spotlight on the positive effects of the ladybird Harmonia axyridis on agriculture. BioControl 2017, 62, 319–330. [Google Scholar] [CrossRef]
  6. Wang, Y.S.; Yao, F.L.; Soares, M.A.; Basiri, S.E.; Amiens-Desneux, E.; Campos, M.R.; Lavoir, A.-V.; Desneux, N. Effects of four non-crop plants on life history traits of the lady beetle Harmonia axyridis. Entomol. Gen. 2020, 40, 243–252. [Google Scholar] [CrossRef]
  7. Thomine, E.; Rusch, A.; Supplisson, C.; Monticelli, L.S.; Amiens-Desneux, E.; Lavoir, A.-V.; Desneux, N. Highly diversified crop systems can promote the dispersal and foraging activity of the generalist predator Harmonia axyridis. Entomol. Gen. 2020, 40, 133–145. [Google Scholar] [CrossRef] [Green Version]
  8. Wells, M.L.; McPherson, R.M.; Ruberson, J.R.; Herzog, G.A. Coccinellids in cotton: Population response to pesticide application and feeding response to cotton aphids (Homoptera: Aphididae). Environ. Entomol. 2001, 4, 785–793. [Google Scholar] [CrossRef]
  9. Ali, A.; Desneux, N.; Lu, Y.H.; Liu, B.; Wu, K.M. Characterization of the natural enemy community attacking cotton aphid in the Bt cotton ecosystem in Northern China. Sci. Rep. 2016, 6, 24273. [Google Scholar] [CrossRef]
  10. González-Mas, N.; Cuenca-Medina, M.; Gutiérrez-Sánchez, F.; Quesada-Moraga, E. Bottom-up effects of endophytic Beauveria bassiana on multitrophic interactions between the cotton aphid, Aphis gossypii, and its natural enemies in melon. J. Pest Sci. 2019, 92, 1271–1281. [Google Scholar] [CrossRef] [Green Version]
  11. Henneberry, T.; Jech, L.F.; Torre, T.; Hendrix, D. Cotton aphid (Homoptera: Aphididae) biology, honeydew production, sugar quality and quantity, and relationships to sticky cotton. Southwest. Entomol. 2000, 25, 161–174. [Google Scholar] [CrossRef]
  12. Campolo, O.; Chiera, E.; Malacrinò, A.; Laudani, F.; Fontana, A.; Albanese, G.R.; Palmeri, V. Acquisition and transmission of selected CTV isolates by Aphis gossypii. J. Asia-Pac. Entomol. 2014, 17, 493–498. [Google Scholar] [CrossRef]
  13. Yousaf, H.K.; Shan, T.S.; Chen, X.W.; Ma, K.S.; Shi, X.Y.; Desneux, N.; Biondi, A.; Gao, X.W. Impact of the secondary plant metabolite Cucurbitacin B on the demographical traits of the melon aphid, Aphis gossypii. Sci. Rep. 2018, 8, 16473. [Google Scholar] [CrossRef]
  14. 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]
  15. Roh, H.S.; Kim, J.; Shin, E.-S.; Lee, D.W.; Choo, H.Y.; Park, C.G. Bioactivity of sandalwood oil (Santalum austrocaledonicum) and its main components against the cotton aphid, Aphis gossypii. J. Pest Sci. 2015, 88, 621–627. [Google Scholar] [CrossRef]
  16. Ullah, F.; Gul, H.; Desneux, N.; Tariq, K.; Ali, A.; Gao, X.W.; Song, D.L. 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. Ullah, F.; Gul, H.; Desneux, N.; Qu, Y.Y.; Xiao, X.; Khattak, A.M.; Gao, X.W.; Song, D.L. Acetamiprid-induced hormetic effects and vitellogenin gene (Vg) expression in the melon aphid, Aphis gossypii. Entomol. Gen. 2019, 39, 259–270. [Google Scholar] [CrossRef]
  18. Lu, Y.H.; Wu, K.M.; Jiang, Y.Y.; Guo, Y.Y.; Desneux, N. Widespread adoption of Bt cotton and insecticide decrease promotes biocontrol services. Nature 2012, 487, 362–365. [Google Scholar] [CrossRef]
  19. Fan, Y.J.; Kang, Z.J.; Wang, Z.C.; Campos, M.; Desneux, N.; Shi, X.Y. Quercetin and paraoxon induction of hydrolases activities in cotton bollworm and malathion-susceptible and resistant housefly. Entomol. Gen. 2018, 38, 157–171. [Google Scholar] [CrossRef]
  20. Gul, H.; Ullah, F.; Biondi, A.; Desneux, N.; Qian, D.; Gao, X.W.; Song, D.L. Resistance against clothianidin and associated fitness costs in the chive maggot, Bradysia odoriphaga. Entomol. Gen. 2019, 39, 81–92. [Google Scholar] [CrossRef]
  21. Zhou, K.; Huang, J.K.; Deng, X.Z.; Werf, W.V.; Zhang, W.; Lu, Y.H.; Wu, K.M.; Wu, F. Effects of land use and insecticides on natural enemies of aphids in cotton: First evidence from smallholder agriculture in the North China Plain. Agric. Ecosyst. Environ. 2014, 183, 176–184. [Google Scholar] [CrossRef]
  22. Babcock, J.M.; Gerwick, C.B.; Huang, J.X.; Loso, M.R.; Nakamura, G.; Nolting, S.P.; Rogers, R.B.; Sparks, T.C.; Thomas, J.; Watson, G.B.; et al. Biological characterization of sulfoxaflor, a novel insecticide. Pest Manag. Sci. 2011, 67, 328–334. [Google Scholar] [CrossRef] [PubMed]
  23. Jeschke, P.; Nauen, R.; Schindler, M.; Elbert, A. Overview of the status and global strategy for neonicotinoids. J. Agric. Food Chem. 2011, 59, 2897–2908. [Google Scholar] [CrossRef]
  24. Bass, C.; Denholm, I.; Williamson, M.S.; Nauen, R. The global status of insect resistance to neonicotinoid insecticides. Pestic. Biochem. Phys. 2015, 121, 78–87. [Google Scholar] [CrossRef] [Green Version]
  25. Cui, L.; Zhang, J.; Qi, H.L.; Wang, Q.Q.; Lu, Y.H.; Rui, C.H. Monitoring and mechanisms of imidacloprid resistance in Aphis gossypii (Hemiptera: Aphididae) in the main cotton production areas of China. Acta Entomol. Sin. 2016, 59, 1246–1253. [Google Scholar] [CrossRef]
  26. Ullah, F.; Gul, H.; Desneux, N.; Gao, X.W.; Song, D.L. Imidacloprid-induced hormesis effects on demographic traits of the melon aphid, Aphis gossypii. Entomol. Gen. 2019, 39, 325–337. [Google Scholar] [CrossRef]
  27. Wu, K.M.; Guo, Y.Y. The evolution of cotton pest management practices in China. Annu. Rev. Entomol. 2005, 50, 31–52. [Google Scholar] [CrossRef] [PubMed]
  28. Liu, Z.W.; Williamson, M.S.; Lansdell, S.J.; Denholm, I.; Han, Z.J.; Millar, N.S. A nicotinic acetylcholine receptor mutation conferring target-site resistance to imidacloprid in Nilaparvata lugens (brown planthopper). Proc. Natl. Acad. Sci. USA. 2005, 102, 8420–8425. [Google Scholar] [CrossRef] [Green Version]
  29. Carletto, J.; Martin, T.; Vanlerberghe-Masutti, F.; Brévault, T. Insecticide resistance traits differ among and within host races in Aphis gossypii. Pest Manag. Sci. 2010, 66, 301–307. [Google Scholar] [CrossRef]
  30. Zhu, Y.; Loso, M.R.; Watson, G.B.; Sparks, T.C.; Rogers, R.B.; Huang, J.X.; Gerwick, C.; Babcock, J.M.; Kelley, D.; Hegde, V.B.; et al. Discovery and characterization of sulfoxaflor, a novel insecticide targeting sap-feeding pests. J. Agric. Food Chem. 2011, 59, 2950–2957. [Google Scholar] [CrossRef]
  31. Sparks, T.C.; Watson, G.B.; Loso, M.R.; Geng, C.; Babcock, J.M.; Thomas, J.D. Sulfoxaflor and the sulfoximine insecticides: Chemistry, mode of action and basis for efficacy on resistant insects. Pestic. Biochem. Phys. 2013, 107, 1–7. [Google Scholar] [CrossRef] [Green Version]
  32. Longhurst, C.; Babcock, J.M.; Denholm, I.; Gorman, K.; Thomas, J.D.; Sparks, T.C. Cross-resistance relationships of the sulfoximine insecticide sulfoxaflor with neonicotinoids and other insecticides in the whiteflies Bemisia tabaci and Trialeurodes vaporariorum. Pest Manag. Sci. 2013, 69, 809–813. [Google Scholar] [CrossRef] [PubMed]
  33. Mansour, R.; Belzunces, L.P.; Suma, P.; Zappalà, L.; Mazzeo, G.; Grissa-Lebdi, K.; Rosso, A.; Biondi, A. Vine and citrus mealybug pest control based on synthetic chemicals. A review. Agron. Sustain. Dev. 2018, 38, 37. [Google Scholar] [CrossRef] [Green Version]
  34. Horowitz, A.R.; Ghanim, M.; Roditakis, E.; Nauen, R.; Ishaaya, I. Insecticide resistance and its management in Bemisia tabaci species. J. Pest Sci. 2020, 93, 893–910. [Google Scholar] [CrossRef]
  35. Watson, G.B.; Loso, M.R.; Babcock, J.M.; Hasler, J.M.; Letherer, T.J.; Young, C.D.; Zhu, Y.M.; Casida, J.E.; Sparks, T.C. Novel nicotinic action of the sulfoximine insecticide sulfoxaflor. Insect Biochem. Mol. Biol. 2011, 41, 432–439. [Google Scholar] [CrossRef]
  36. Cutler, P.; Slater, R.; Edmunds, A.J.; Maienfisch, P.; Hall, R.G.; Earley, F.G.; Pitterna, T.; Pal, S.; Paul, V.-L.; Goodchild, J.; et al. Investigating the mode of action of sulfoxaflor: A fourth-generation neonicotinoid. Pest Manag. Sci. 2012, 69, 607–619. [Google Scholar] [CrossRef]
  37. Guo, S.-K.; Gong, Y.-J.; Chen, J.-C.; Shi, P.; Cao, L.-J.; Yang, Q.; Hofmann, A.A.; Wei, S.-J. Increased density of endosymbiotic Buchnera related to pesticide resistance in yellow morph of melon aphid. J. Pest Sci. 2020, 93, 1281–1294. [Google Scholar] [CrossRef]
  38. Chagnon, M.; Kreutzweiser, D.; Mitchell, E.A.; Morrissey, C.A.; Noome, D.A.; Van der Sluijs, J.P. Risks of large-scale use of systemic insecticides to ecosystem functioning and services. Environ. Sci. Pollut. Res. 2015, 22, 119–134. [Google Scholar] [CrossRef] [Green Version]
  39. 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]
  40. Cloyd, R.A.; Bethke, J.A. Impact of neonicotinoid insecticides on natural enemies in greenhouse and interiorscape environments. Pest Manag. Sci. 2011, 67, 3–9. [Google Scholar] [CrossRef]
  41. Decourtye, A.; Henry, M.; Desneux, N. Overhaul pesticide testing on bees. Nature 2013, 497, 188. [Google Scholar] [CrossRef] [PubMed]
  42. Elbert, A.; Haas, M.; Springer, B.; Thielert, W.; Nauen, R. Applied aspects of neonicotinoid uses in crop protection. Pest Manag. Sci. 2008, 64, 1099–1105. [Google Scholar] [CrossRef] [PubMed]
  43. Goulson, D. An overview of the environmental risks posed by neonicotinoid insecticides. J. Appl. Ecol. 2013, 50, 977–987. [Google Scholar] [CrossRef]
  44. Menail, A.H.; Boutefnouchet-Bouchema, W.F.; Haddad, N.; Taning, C.N.; Smagghe, G.; Loucif-Ayad, W. Effects of thiamethoxam and spinosad on the survival and hypopharyngeal glands of the African honey bee (Apis mellifera intermissa). Entomol. Gen. 2020, 40, 207–215. [Google Scholar] [CrossRef]
  45. Yang, L.; Zhang, Q.; Liu, B.; Zeng, Y.D.; Pan, Y.F.; Li, M.L.; Lu, Y.H. Mixed effects of landscape complexity and insecticide use on ladybeetle abundance in wheat fields. Pest Manag. Sci. 2019, 75, 1638–1645. [Google Scholar] [CrossRef] [PubMed]
  46. Butler, D. EU expected to vote on pesticide ban after major scientific review. Nature 2018, 555, 150–151. [Google Scholar] [CrossRef] [PubMed]
  47. Youn, Y.-N.; Seo, M.; Shin, J.; Jang, C.; Yu, Y. Toxicity of greenhouse pesticides to multicolored Asian lady beetles, Harmonia axyridis (Coleoptera: Coccinellidae). Biol. Control 2003, 28, 164–170. [Google Scholar] [CrossRef]
  48. Biondi, A.; Zappalà, L.; Stark, J.D.; Desneux, N. Do biopesticides affect the demographic traits of a parasitoid wasp and its biocontrol services through sublethal effects? PLoS ONE 2013, 8, e76548. [Google Scholar] [CrossRef] [Green Version]
  49. Yao, F.-L.; Zheng, Y.; Zhao, J.-W.; Desneux, N.; He, Y.-X.; Weng, Q.-Y. Lethal and sublethal effects of thiamethoxam on the whitefly predator Serangium japonicum (Coleoptera: Coccinellidae) through different exposure routes. Chemosphere 2015, 128, 49–55. [Google Scholar] [CrossRef]
  50. Biondi, A.; Desneux, N.; Siscaro, G.; Zappalà, L. Using organic-certified rather than synthetic pesticides may not be safer for biological control agents: Selectivity and side effects of 14 pesticides on the predator Orius laevigatus. Chemosphere 2012, 87, 803–812. [Google Scholar] [CrossRef]
  51. Biondi, A.; Campolo, O.; Desneux, N.; Siscaro, G.; Palmeri, V.; Zappalà, L. Life stage-dependent susceptibility of Aphytis melinus DeBach (Hymenoptera: Aphelinidae) to two pesticides commonly used in citrus orchards. Chemosphere 2015, 128, 142–147. [Google Scholar] [CrossRef]
  52. Passos, L.C.; Soares, M.A.; Collares, L.J.; Malagoli, I.; Desneux, N.; Carvalho, G.A. Lethal, sublethal and transgenerational effects of insecticides on Macrolophus basicornis, predator of Tuta absoluta. Entomol. Gen. 2018, 38, 127–143. [Google Scholar] [CrossRef]
  53. Taning, N.T.C.; Vanommeslaeghe, A.; Smagghe, G. With or without foraging for food, field-realistic concentrations of sulfoxaflor are equally toxic to bumblebees (Bombus terrestris). Entomol. Gen. 2019, 39, 151–155. [Google Scholar] [CrossRef]
  54. Calvo-Agudo, M.; González-Cabrera, J.; Picó, Y.; Calatayud-Vernich, P.; Urbaneja, A.; Dicke, M.; Tena, A. Neonicotinoids in excretion product of phloem-feeding insects kill beneficial insects. Proc. Natl. Acad. Sci. USA 2019, 116, 16817–16822. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  55. Tan, Y.; Biondi, A.; Desneux, N.; Gao, X.-W. Assessment of physiological sublethal effects of imidacloprid on the mirid bug Apolygus lucorum (Meyer-Dür). Ecotoxicology 2012, 21, 1989–1997. [Google Scholar] [CrossRef]
  56. He, Y.X.; Zhao, J.W.; Zheng, Y.; Weng, Q.Y.; Biondi, A.; Desneux, N.; Wu, K.M. Assessment of potential sublethal effects of various insecticides on key biological traits of the tobacco whitefly, Bemisia tabaci. Int. J. Biol. Sci. 2013, 9, 246–255. [Google Scholar] [CrossRef] [Green Version]
  57. Guedes, R.N.C.; Smagghe, G.; Stark, J.D.; Desneux, N. Pesticide-induced stress in arthropod pests for optimized integrated pest management programs. Annu. Rev. Entomol. 2016, 61, 43–62. [Google Scholar] [CrossRef] [Green Version]
  58. Oliveira, R.L.; Gontijo, P.C.; Sâmia, R.R.; Carvalho, G.A. Long-term effects of chlorantraniliprole reduced risk insecticide applied as seed treatment on lady beetle Harmonia axyridis (Coleoptera: Coccinellidae). Chemosphere 2019, 219, 678–683. [Google Scholar] [CrossRef] [PubMed]
  59. Wang, P.; Zhou, L.L.; Yang, F.; Liu, X.M.; Wang, Y.; Lei, C.L.; Si, S.Y. Lethal and behavioral sublethal side effects of thiamethoxam on the predator Harmonia axyridis. Entomol. Exp. Appl. 2018, 166, 703–712. [Google Scholar] [CrossRef]
  60. Qu, Y.Y.; Xiao, D.; Li, J.Y.; Chen, Z.; Biondi, A.; Desneux, N.; Gao, X.W.; Song, D.L. Sublethal and hormesis effects of imidacloprid on the soybean aphid Aphis glycines. Ecotoxicology 2015, 24, 479–487. [Google Scholar] [CrossRef] [PubMed]
  61. Dai, C.C.; Ricupero, M.; Puglisi, R.; Lu, Y.H.; Desneux, N.; Biondi, A.; Zappalà, L. Can contamination by major systemic insecticides affect the voracity of the harlequin ladybird? Chemosphere 2020, 256, 126986. [Google Scholar] [CrossRef]
  62. Ricupero, M.; Dai, C.C.; Siscaro, G.; Russo, A.; Biondi, A.; Zappalà, L. Potential diet regimens for laboratory rearing of the harlequin ladybird. BioControl 2020, 65, 583–592. [Google Scholar] [CrossRef]
  63. Finney, D.J. Probit Analysis: A Statistical Treatment of The Sigmoid Response Curve; Macmillan: Oxford, UK, 1947. [Google Scholar]
  64. Skouras, P.J.; Brokaki, M.; Stathas, G.J.; Demopoulos, V.; Louloudakis, G.; Margaritopoulos, J.T. Lethal and sub-lethal effects of imidacloprid on the aphidophagous coccinellid Hippodamia variegata. Chemosphere 2019, 229, 392–400. [Google Scholar] [CrossRef]
  65. Papachristos, D.P.; Milonas, P.G. Adverse effects of soil applied insecticides on the predatory coccinellid Hippodamia undecimnotata (Coleoptera: Coccinellidae). Biol. Control 2008, 47, 77–81. [Google Scholar] [CrossRef]
  66. Rahmani, S.; Bandani, A.R. Sublethal concentrations of thiamethoxam adversely affect life table parameters of the aphid predator, Hippodamia variegata (Goeze) (Coleoptera: Coccinellidae). Crop. Prot. 2013, 54, 168–175. [Google Scholar] [CrossRef]
  67. Jiang, J.G.; Zhang, Z.Q.; Yu, X.; Yu, C.H.; Liu, F.; Mu, W. Sublethal and transgenerational effects of thiamethoxam on the demographic fitness and predation performance of the seven-spot ladybeetle Coccinella septempunctata L. (Coleoptera: Coccinellidae). Chemosphere. 2019, 216, 168–178. [Google Scholar] [CrossRef] [PubMed]
  68. Yu, C.H.; Lin, R.H.; Fu, M.R.; Zhou, Y.M.; Zong, F.L.; Jiang, H.; Lv, N.; Piao, X.Y.; Zhang, J.; Liu, Y.Q.; et al. Impact of imidacloprid on life-cycle development of Coccinella septempunctata in laboratory microcosms. Ecotoxicol. Environ. Saf. 2014, 110, 168–173. [Google Scholar] [CrossRef] [PubMed]
  69. Xiao, D.; Zhao, J.; Guo, X.J.; Chen, H.Y.; Qu, M.M.; Zhai, W.G.; Desneux, N.; Biondi, A.; Zhang, F.; Wang, S. Sublethal effects of imidacloprid on the predatory seven-spot ladybird beetle Coccinella septempunctata. Ecotoxicology 2016, 25, 1782–1793. [Google Scholar] [CrossRef] [PubMed]
  70. Guedes, R.N.C.; Walse, S.S.; Throne, J.E. Sublethal exposure, insecticide resistance, and community stress. Curr. Opin. Insect Sci. 2017, 21, 47–53. [Google Scholar] [CrossRef] [Green Version]
  71. Wang, S.Y.; Qi, Y.F.; Desneux, N.; Shi, X.Y.; Biondi, A.; Gao, X.W. Sublethal and transgenerational effects of short-term and chronic exposures to the neonicotinoid nitenpyram on the cotton aphid Aphis gossypii. J. Pest Sci. 2017, 90, 389–396. [Google Scholar] [CrossRef]
  72. Sâmia, R.R.; Gontijo, P.C.; Oliveira, R.L.; Carvalho, G.A. Sublethal and transgenerational effects of thiamethoxam applied to cotton seed on Chrysoperla externa and Harmonia axyridis. Pest Manag. Sci. 2018, 75, 694–701. [Google Scholar] [CrossRef]
  73. Qin, D.Q.; Liu, B.J.; Zhang, P.W.; Zheng, Q.; Luo, P.R.; Ye, C.Y.; Zhao, W.H. Treating green pea aphids, Myzus persicae, with azadirachtin affects the predatory ability and protective enzyme activity of harlequin ladybirds, Harmonia axyridis. Ecotoxicol. Environ. Saf. 2021, 212, 111984. [Google Scholar] [CrossRef] [PubMed]
  74. Ziolkowska, E.; Topping, C.J.; Bednarska, A.J.; Laskowski, R. Supporting non-target arthropods in agroecosystems: Modelling effects of insecticides and landscape structure on carabids in agricultural landscapes. Sci. Total Environ. 2021, 774, 145746. [Google Scholar] [CrossRef] [PubMed]
  75. Ricupero, M.; Abbes, K.; Haddi, K.; Kurtulus, A.; Desneux, N.; Russo, A.; Siscaro, G.; Biondi, A.; Zappalà, L. Combined thermal and insecticidal stresses on the generalist predator Macrolophus pygmaeus. Sci. Total Environ. 2020, 729, 138922. [Google Scholar] [CrossRef] [PubMed]
Insects 12 00681 g001 550
Figure 1. Mean (±SE) of percentage mortality of Harmonia axyridis females exposed to imidacloprid and sulfoxaflor and their LC50 and LC20 estimated for the target pest, Aphis gossypii. Columns bearing the different letter (capital letters: within the same concentration regime; lowercase letters: within the same tested insecticide) are significantly different (Tukey’s HSD test for multiple comparisons at p < 0.05).
Figure 1. Mean (±SE) of percentage mortality of Harmonia axyridis females exposed to imidacloprid and sulfoxaflor and their LC50 and LC20 estimated for the target pest, Aphis gossypii. Columns bearing the different letter (capital letters: within the same concentration regime; lowercase letters: within the same tested insecticide) are significantly different (Tukey’s HSD test for multiple comparisons at p < 0.05).
Insects 12 00681 g001
Table
Table 1. Formulation, field-recommended concentration and manufacturer of two insecticides tested for their side effects on Harmonia axyridis.
Table 1. Formulation, field-recommended concentration and manufacturer of two insecticides tested for their side effects on Harmonia axyridis.
Chemical ClassesActive IngredientIRAC
Group		FormulationField-Recommended
Dose (g a.i. ha−1/ppm)		Manufacturer
% of a.i.Type
Neonicotinoidsimidacloprid4A70WG31.5/70Bayer Crop Science (China) Company Limited
Sulfoximinessulfoxaflor4C22SC49.5/110Dow AgroSciences (Repacking units: Jiangsu Suzhou Jiahui Chemical Company Limited)
Note: a.i. = active ingredient. WG = wettable granules. SC = suspension concentrate. ppm = mg a.i. L−1.
Table
Table 2. Baseline toxicity results following contact exposure of two insecticides against Aphis gossypii adults.
Table 2. Baseline toxicity results following contact exposure of two insecticides against Aphis gossypii adults.
InsecticideRegression Equation of
Toxicity		χ2ndfpLC20 (ppm)
(95% Fiducial Limits)		LC50 (ppm)
(95% Fiducial Limits)
ImidaclopridY = 2.670 ± 1.561X14.3930280.9843.93 (2.85–5.07)13.62 (11.34–16.15)
SulfoxaflorY = 1.941 ± 1.742X10.5330280.9995.56 (4.37–6.77)16.90 (14.44–19.80)
Table
Table 3. Mean (±SE) values of longevity and fecundity of Harmonia axyridis females exposed to imidacloprid and sulfoxaflor and their LC50 and LC20 estimated for the target pest, Aphis gossypii. Values followed by different letters, within the same column, indicate significant differences at p < 0.05 level.
Table 3. Mean (±SE) values of longevity and fecundity of Harmonia axyridis females exposed to imidacloprid and sulfoxaflor and their LC50 and LC20 estimated for the target pest, Aphis gossypii. Values followed by different letters, within the same column, indicate significant differences at p < 0.05 level.
TreatmentLongevity
(d)		Fecundity in 30 Days
(Eggs Per Female)		Egg-Laying Females
(%)
Control102.01 ± 5.81 bc694.77 ± 37.96 a97.22 ± 1.94 a
imidacloprid LC20111.10 ± 8.15 abc531.81 ± 44.80 bc72.55 ± 4.42 bc
imidacloprid LC5092.91 ± 7.21 c432.75 ± 41.18 c52.46 ± 4.52 d
sulfoxaflor LC20117.94 ± 8.83 a595.55 ± 37.42 ab79.38 ± 4.22 b
sulfoxaflor LC50115.66 ± 8.97 ab507.71 ± 42.32 bc60.00 ± 4.67 cd
Table
Table 4. Mean (±SE) values of egg-hatchability, larval and pupal survival of the offspring of Harmonia axyridis females exposed to imidacloprid and sulfoxaflor and their LC50 and LC20 estimated for the target pest, Aphis gossypii. Values followed by different letters, within the same column, indicate significant differences at p < 0.05 level.
Table 4. Mean (±SE) values of egg-hatchability, larval and pupal survival of the offspring of Harmonia axyridis females exposed to imidacloprid and sulfoxaflor and their LC50 and LC20 estimated for the target pest, Aphis gossypii. Values followed by different letters, within the same column, indicate significant differences at p < 0.05 level.
TreatmentEgg Hatchability
(%)		Larval Survival
(%)		Pupal Survival
(%)
Control81.81 ± 2.92 a82.67 ± 3.09 ab99.19 ± 0.80 a
imidacloprid LC2071.75 ± 2.93 abc76.67 ± 3.45 bc94.78 ± 2.07 b
imidacloprid LC5061.26 ± 3.39 c68.00 ± 3.81 c99.02 ± 0.98 ab
sulfoxaflor LC2076.86 ± 2.23 ab86.00 ± 2.83 a97.67 ± 1.33 ab
sulfoxaflor LC5062.33 ± 3.91 c71.33 ± 3.69 c94.39 ± 2.22 b
Table
Table 5. Mean (±SE) values of stage-specific developmental duration of the progeny of Harmonia axyridis females exposed to imidacloprid and sulfoxaflor and their LC50 and LC20 estimated for the target pest, Aphis gossypii. Values followed by different letters, within the same column, indicate significant differences at p < 0.05 level.
Table 5. Mean (±SE) values of stage-specific developmental duration of the progeny of Harmonia axyridis females exposed to imidacloprid and sulfoxaflor and their LC50 and LC20 estimated for the target pest, Aphis gossypii. Values followed by different letters, within the same column, indicate significant differences at p < 0.05 level.
TreatmentEgg (d)Larva (d)Pupa (d)
Control2.90 ± 0.03 c12.40 ± 0.12 c4.29 ± 0.04 ab
imidacloprid LC203.00 ± 0.01 b13.69 ± 0.22 b4.18 ± 0.04 b
imidacloprid LC502.99 ± 0.02 bc14.77 ± 0.33 a4.35 ± 0.04 ab
sulfoxaflor LC202.91 ± 0.03 bc12.76 ± 0.15 c4.25 ± 0.05 b
sulfoxaflor LC503.19 ± 0.03 a14.50 ± 0.24 ab4.44 ± 0.05 a
Table
Table 6. Mean (±SE) values of stage-specific larval developmental duration of the progeny of Harmonia axyridis females exposed to imidacloprid and sulfoxaflor and their LC50 and LC20 estimated for the target pest, Aphis gossypii. Values followed by different letters, within the same column, indicate significant differences at p < 0.05 level.
Table 6. Mean (±SE) values of stage-specific larval developmental duration of the progeny of Harmonia axyridis females exposed to imidacloprid and sulfoxaflor and their LC50 and LC20 estimated for the target pest, Aphis gossypii. Values followed by different letters, within the same column, indicate significant differences at p < 0.05 level.
Treatment1st Instar (d)2nd Instar (d)3rd Instar (d)4th Instar (d)
Control2.16 ± 0.04 c2.11 ± 0.06 ab2.68 ± 0.06 b5.49 ± 0.07 c
imidacloprid LC202.65 ± 0.10 a2.13 ± 0.07 ab2.69 ± 0.07 b6.23 ± 0.14 b
imidacloprid LC502.61 ± 0.12 ab2.30 ± 0.09 a3.02 ± 0.09 a6.76 ± 0.15 a
sulfoxaflor LC202.33 ± 0.05 bc1.88 ± 0.05 b2.47 ± 0.06 b6.09 ± 0.14 b
sulfoxaflor LC502.17 ± 0.04 c2.25 ± 0.07 a3.24 ± 0.10 a6.95 ± 0.16 a
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Dai, C.; Ricupero, M.; Wang, Z.; Desneux, N.; Biondi, A.; Lu, Y. Transgenerational Effects of a Neonicotinoid and a Novel Sulfoximine Insecticide on the Harlequin Ladybird. Insects 2021, 12, 681. https://doi.org/10.3390/insects12080681

AMA Style

Dai C, Ricupero M, Wang Z, Desneux N, Biondi A, Lu Y. Transgenerational Effects of a Neonicotinoid and a Novel Sulfoximine Insecticide on the Harlequin Ladybird. Insects. 2021; 12(8):681. https://doi.org/10.3390/insects12080681

Chicago/Turabian Style

Dai, Changchun, Michele Ricupero, Zequn Wang, Nicolas Desneux, Antonio Biondi, and Yanhui Lu. 2021. "Transgenerational Effects of a Neonicotinoid and a Novel Sulfoximine Insecticide on the Harlequin Ladybird" Insects 12, no. 8: 681. https://doi.org/10.3390/insects12080681

APA Style

Dai, C., Ricupero, M., Wang, Z., Desneux, N., Biondi, A., & Lu, Y. (2021). Transgenerational Effects of a Neonicotinoid and a Novel Sulfoximine Insecticide on the Harlequin Ladybird. Insects, 12(8), 681. https://doi.org/10.3390/insects12080681

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