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Integrated pest management is focused on combining biological and chemical controls. There is evidence of a negative impact of neonicotinoids on biological control, however, sulfoxaflor (SFX), a novel insecticide, its impact on parasitoid natural predator remain limited. Binodoxys communis is an important parasitic natural enemy of Aphis gossypii, which may have direct and indirect toxicity from the insecticides and aphids. Understanding the potential threat of SFX to B. communis is therefore essential to integrated pest management and the conservation of parasitoids. Here, the effects of sublethal doses of SFX on B. communis larvae and adults are presented for the first time. Sublethal SFX doses had a significant negative effect on the survival rate, adult life span, duration of development, and rate of parasitism. Moreover, exposure to sublethal SFX doses also had adverse effects on the biological performance of the next generation of B. communis. Based on the transcriptome analysis, the expression of genes involved in fatty acid metabolism, glycerolipid metabolism, glycerophospholipid metabolism, peroxidase, lysosomes, glutathione metabolism, drug metabolism, and CYP450 were significantly shifted by sublethal SFX exposure. These results indicate that sublethal SFX doses might adversely affect the biological performance of B. communis by altering gene expression related to the function of detoxification systems and energy metabolism. In conclusion, considering the beneficial ecological services of provided by parasitoids and the negative effects of sulfoxaflor across a greater usage scale, we emphasize the importance to optimize pesticide applications in IPM packages, in order to ensure the safety and survival of natural pest parasitoids.

While genetically modified (GM) crops bring economic benefits to human beings, their impact on non-target organisms has become an important part of environmental safety assessments. Symbiotic bacteria play an important role in eukaryotic biological functions and can adjust host communities to adapt to new environments. Therefore, this study examined the effects of Cry1B protein on the growth and development of non-target natural enemies of Pardosa astrigera (L. Koch) from the perspective of symbiotic bacteria. Cry1B protein had no significant effect on the health indicators of P. astrigera (adults and 2nd instar spiderlings). 16S rRNA sequencing results revealed that Cry1B protein did not change the symbiotic bacteria species composition of P. astrigera, but did reduce the number of OTU and species diversity. In 2nd instar spiderlings, neither the dominant phylum (Proteobacteria) nor the dominant genus (Acinetobacter) changed, but the relative abundance of Corynebacterium-1 decreased significantly; in adult spiders, the dominant bacteria genera of females and males were different. The dominant bacterial genera were Brevibacterium in females and Corynebacterium-1 in males, but Corynebacterium-1 was the dominant bacteria in both females and males feeding on Cry1B. The relative abundance of Wolbachia also increased significantly. In addition, bacteria in other genera varied significantly by sex. KEGG results showed that Cry1B protein only altered the significant enrichment of metabolic pathways in female spiders. In conclusion, the effects of Cry1B protein on symbiotic bacteria vary by growth and development stage and sex.

Assessing the potential effects of insecticides on beneficial biological control agents is key to facilitating the success of integrated pest management (IPM) approaches. Flupyradifurone (FPF) is a novel neonicotinoid insecticide that is replacing traditional neonicotinoids over a large geographical range to control pests. Binodoxys communis, is the dominant parasitic natural enemy of aphids. To date, no reports have addressed sublethal effects of FPF on B. communis. In this study, the lethal and sublethal effects of FPF on B. communis were investigated by indirect exposure to larvae and direct exposure to adults. Results showed that the sublethal LC10 and LC25 of FPF had negative effects on the biological parameters of B. communis, including significantly reducing survival rate, adult longevity, parasitism rate, and emergence rate, and significantly prolonging the developmental stages from egg to cocoons. In addition, we observed a transgenerational effect of FPF on the next generation (F1). RNA-Seq transcriptomic analysis identified a total of 1429 differentially expressed genes (DEGs) that were significantly changed between FPF-treated and control groups. These DEGs are mainly enriched in metabolic pathways such as peroxisomes, glutamate metabolism, carbon metabolism, fatty acid metabolism, and amino acid metabolism. This report is the first comprehensive evaluation of how FPF effects B. communis, which adds to the methods of assessing pesticide exposure in parasitic natural enemies. We speculate that the significant changes in pathways, especially those related to lipid synthesis, may be the reason for weakened parasitoid biocontrol ability. The present study provides new evidence for the toxic effects and environmental residue risk of FPF.

The lady beetle Propylea japonica is a dominant natural predator of insect pests in farmland ecosystems and an important non-target indicator insect for the environmental safety assessment of GM crops. The commercial cultivation of GM crops may cause P. japonica to frequently be exposed to the Bt protein environment. In this study, the biological characteristics, enzyme activity, and expression levels of detoxification and metabolism in P. japonica were studied after Cry1B protein treatment. No significant differences were observed in developmental duration, emergence rate, or body weight at different ages after feeding larvae 0.5 mg/mL of Cry1B protein compared with the control. Furthermore, there were no significant differences in the activities of glutathione S-transferase (GST), catalase (CAT), and peroxidase (POD) after feeding 0.25 mg/mL and 0.5 mg/mL Cry1B protein. However, when the concentration of Cry1B protein increased to 1.0 mg/mL, the activities of the GST, CAT, and POD increased significantly. Compared with the control group, there were no significant differences in the expression levels of most detoxification metabolism related genes; only a few genes had changed expression levels at the individual concentrations (CYP345B1, CYP4Q2, CYP9F2, GST, and microsomal GST). Overall, these results suggest that Cry1B protein has little or no effect on the biological characteristics of P. japonica. Genes related to enzyme activity and detoxification are differentially expressed at high concentration stimulation. Therefore, this research suggests that the potential risks of Cry1B for the predator P. japonica are negligible.

The large-scale commercial cultivation of genetically modified (GM) cotton has brought significant economic and environmental benefits. However, GM crops must undergo strict environmental monitoring and long-term observation. An important natural enemy insect in cotton fields, Geocoris pallidipennis, can ingest the Bt protein expressed in GM cotton by feeding on herbivorous insects that feed on the cotton. However, the potential risk of GM cotton to G. pallidipennis is still unclear. We here evaluated the effects of Bt cotton expressing the Cry1Ac/1Ab protein on nymphs and adults G. pallidipennis. Cry1Ac protein was detected in the midgut of the cotton bollworm, Helicoverpa armigera, after it ingested Bt cotton, and in the midgut of G. pallidipennis nymphs and adults preying on Bt-fed H. armigera. However, the survival rate, growth, development, and fecundity of G. pallidipennis were not adversely affected. Furthermore, G. pallidipennis cadherins, and those genes related to detoxification, antioxidant activity, nutrient utilization, and immune function were not differentially expressed in response to Cry1Ac exposure. Finally, we showed that Cry1Ac could not bind to brush border membrane vesicles (BBMV) proteins in G. pallidipennis nymphs or adults. In summary, these results indicate that the potential negative effect of transgenic Cry1Ac/1Ab cotton on the insect redator G. pallidipennis is negligible.