{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,23]],"date-time":"2026-09-23T05:04:03Z","timestamp":1790139843100,"version":"4.0.1"},"reference-count":49,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2026,9,21]],"date-time":"2026-09-21T00:00:00Z","timestamp":1789948800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Natural Science Foundation of Henan Province","award":["202300410105"],"award-info":[{"award-number":["202300410105"]}]},{"name":"Postdoctoral Fund of Henan University of Technology","award":["21450059"],"award-info":[{"award-number":["21450059"]}],"id":[{"id":"https:\/\/ror.org\/05sbgwt55","id-type":"ROR","asserted-by":"crossref"}]},{"award":["21450059"],"award-info":[{"award-number":["21450059"]}],"id":[{"id":"https:\/\/ror.org\/05sbgwt55","id-type":"ROR","asserted-by":"publisher"}]},{"name":"Key Scientific and Technological Project of Henan Province","award":["262102110339"],"award-info":[{"award-number":["262102110339"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Insects"],"abstract":"<jats:p>Aphis spiraecola is a major pest of fruit trees worldwide, causing significant yield reductions and economic losses in apple production. Chemical control remains the primary and most effective method for managing A. spiraecola in the field. Imidacloprid, the first neonicotinoid insecticide, effectively targets piercing\u2013sucking pests. However, the time-dependent response of A. spiraecola to imidacloprid exposure has not been well characterized. In this study, we assessed the susceptibility of an A. spiraecola population from Zhengzhou to imidacloprid. Enzymatic assays revealed that the activities of cytochrome P450s, glutathione S-transferases (GSTs), and carboxylesterases (CarEs) were significantly increased following imidacloprid treatment. A synergism assay further demonstrated that the P450 inhibitor PBO and the CarE inhibitor TPP significantly enhanced the imidacloprid toxicity against A. spiraecola. Transcriptome analysis revealed that LC50 imidacloprid treatment induced time-dependent changes in gene expression at 12, 24, and 36 h. A total of 46 P450 genes, 42 esterase genes, and six GST genes were identified in the transcriptome of A. spiraecola. Five detoxification enzyme genes, CYP380C6, CYP6CY19, GSTS3, GSTL, and CarE6, were significantly overexpressed, as confirmed by both transcriptomic and qPCR analysis. Moreover, RNAi-mediated knockdown of CYP6CY19 and CarE6 substantially increased aphid sensitivity to imidacloprid compared with the dsGFP control group. These results demonstrate that CYP6CY19 and CarE6 play an important roles in determining A. spiraecola susceptibility to imidacloprid. Our findings provide a theoretical basis for the rational and scientific use of imidacloprid in aphid management.<\/jats:p>","DOI":"10.3390\/insects17090973","type":"journal-article","created":{"date-parts":[[2026,9,22]],"date-time":"2026-09-22T17:56:41Z","timestamp":1790099801000},"page":"973","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Transcriptome Analysis and Characterization of Two Detoxification Genes Responding to Imidacloprid in Aphis spiraecola"],"prefix":"10.3390","volume":"17","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-3811-2801","authenticated-orcid":false,"given":"Meng","family":"Zhang","sequence":"first","affiliation":[{"name":"School of Food and Strategic Reserves, Henan University of Technology, Zhengzhou 450001, China"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"conceptualization","vocabulary":"credit"},{"role":"investigation","vocabulary":"credit"},{"role":"visualization","vocabulary":"credit"},{"role":"methodology","vocabulary":"credit"},{"role":"software","vocabulary":"credit"},{"role":"resources","vocabulary":"credit"},{"role":"data-curation","vocabulary":"credit"},{"role":"writing-original-draft","vocabulary":"credit"},{"role":"project-administration","vocabulary":"credit"},{"role":"funding-acquisition","vocabulary":"credit"}]},{"given":"Chunping","family":"Si","sequence":"additional","affiliation":[{"name":"School of Food and Strategic Reserves, Henan University of Technology, Zhengzhou 450001, China"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"methodology","vocabulary":"credit"},{"role":"validation","vocabulary":"credit"},{"role":"investigation","vocabulary":"credit"},{"role":"writing-review-editing","vocabulary":"credit"},{"role":"supervision","vocabulary":"credit"}]},{"given":"Hanjie","family":"Liu","sequence":"additional","affiliation":[{"name":"School of Food and Strategic Reserves, Henan University of Technology, Zhengzhou 450001, China"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"methodology","vocabulary":"credit"},{"role":"investigation","vocabulary":"credit"}]},{"given":"Liting","family":"Chai","sequence":"additional","affiliation":[{"name":"School of Food and Strategic Reserves, Henan University of Technology, Zhengzhou 450001, China"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"validation","vocabulary":"credit"},{"role":"investigation","vocabulary":"credit"}]}],"member":"1968","published-online":{"date-parts":[[2026,9,21]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1017\/S0007485323000603","article-title":"Voltage-gated sodium channel gene mutation and P450 gene expression are associated with the resistance of Aphis spiraecola Patch (Hemiptera: Aphididae) to lambda-cyhalothrin","volume":"114","author":"Tang","year":"2024","journal-title":"Bull. Entomol. Res."},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Ilias, A., Skouras, P.J., Kalaitzaki, A., Roditakis, E., Tsirikos, E., Tsagkarakou, A., Vontas, J., and Margaritopoulos, J.T. (2025). Survey and molecular diagnostics of target site mutations conferring resistance to insecticides in populations of Aphis spiraecola from Greece. Insects, 16.","DOI":"10.3390\/insects16121199"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1603\/0046-225X-30.1.44","article-title":"Effects of host plants on biology and life table parameters of Aphis spiraecola (Homoptera: Aphididae)","volume":"30","author":"Tsai","year":"2001","journal-title":"Environ. Entomol."},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Gao, J., Arthurs, S., and Mao, R. (2020). Asymmetric interaction between Aphis spiraecola and Toxoptera citricida on sweet orange induced by pre-infestation. Insects, 11.","DOI":"10.3390\/insects11070414"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"270","DOI":"10.14411\/eje.2015.043","article-title":"Aphis pomi and Aphis spiraecola (Hemiptera: Sternorrhyncha: Aphididae) in Europe\u2014New information on their distribution, molecular and morphological peculiarities","volume":"112","author":"Rakauskas","year":"2015","journal-title":"Eur. J. Entomol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"496","DOI":"10.1093\/jee\/85.2.496","article-title":"Combined effects of spirea aphid (Homoptera: Aphididae) and nitrogen fertilization on shoot growth, dry matter accumulation, and carbohydrate concentration in young apple trees","volume":"85","author":"Kaakeh","year":"1992","journal-title":"J. Econ. Entomol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"106831","DOI":"10.1016\/j.pestbp.2025.106831","article-title":"Overexpression of UDP-glycosyltransferase UGT344B29 and UGT344B30 involved in lambda-cyhalothrin resistance in Aphis spiraecola","volume":"216","author":"You","year":"2026","journal-title":"Pestic. Biochem. Physiol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"381","DOI":"10.1080\/09583157.2013.763904","article-title":"Intercropping with aromatic plants hindered the occurrence of Aphis citricola in an apple orchard system by shifting predator\u2013prey abundances","volume":"23","author":"Song","year":"2013","journal-title":"Biocontrol Sci. Technol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"188","DOI":"10.1093\/jee\/98.1.188","article-title":"Baseline Susceptibilities to Imidacloprid for Green Apple Aphid and Spirea Aphid (Homoptera: Aphididae) Collected from Apple in the Pacific Northwest","volume":"98","author":"Lowery","year":"2005","journal-title":"J. Econ. Entomol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"2112","DOI":"10.1093\/jee\/toaf128","article-title":"Insecticide Resistance Monitoring of Aphis spiraecola (Hemiptera: Aphididae) to Neonicotinoids and Abamectin in a Major Apple-Growing Region","volume":"118","author":"Tang","year":"2025","journal-title":"J. Econ. Entomol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"106289","DOI":"10.1016\/j.pestbp.2025.106289","article-title":"Widespread Resistance of the Apple Aphid Aphis spiraecola to Pyrethroids in China","volume":"208","author":"Wang","year":"2025","journal-title":"Pestic. Biochem. Physiol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1016\/j.pestbp.2018.04.007","article-title":"Neonicotinoid Insecticides Mode of Action on Insect Nicotinic Acetylcholine Receptors Using Binding Studies","volume":"151","author":"Taillebois","year":"2018","journal-title":"Pestic. Biochem. Physiol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"142309","DOI":"10.1016\/j.chemosphere.2024.142309","article-title":"Dissipation behavior and risk assessment of imidacloprid and its metabolites in apple from field to products","volume":"359","author":"Tian","year":"2024","journal-title":"Chemosphere"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1146\/annurev.ento.52.110405.091440","article-title":"The Sublethal Effects of Pesticides on Beneficial Arthropods","volume":"52","author":"Desneux","year":"2007","journal-title":"Annu. Rev. Entomol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"551","DOI":"10.1017\/S0007485316000286","article-title":"Sublethal Effects of Imidacloprid on the Fecundity, Longevity, and Enzyme Activity of Sitobion avenae (Fabricius) and Rhopalosiphum padi (Linnaeus)","volume":"106","author":"Lu","year":"2016","journal-title":"Bull. Entomol. Res."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"248","DOI":"10.1111\/eea.12406","article-title":"Transcriptomic Responses to Different Doses of Cycloxaprid Involved in Detoxification and Stress Response in the Whitebacked Planthopper, Sogatella furcifera","volume":"158","author":"Yang","year":"2016","journal-title":"Entomol. Exp. Appl."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1016\/j.pestbp.2018.11.009","article-title":"Identification and Functional Analysis of a Cytochrome P450 Gene Involved in Imidacloprid Resistance in Bradysia odoriphaga Yang et Zhang","volume":"153","author":"Chen","year":"2019","journal-title":"Pestic. Biochem. Physiol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1400","DOI":"10.1002\/ps.5260","article-title":"Identification of Detoxification Genes in Imidacloprid-Resistant Asian Citrus Psyllid (Hemiptera: Liviidae) and Their Expression Patterns under Stress of Eight Insecticides","volume":"75","author":"Tian","year":"2019","journal-title":"Pest Manag. Sci."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"105014","DOI":"10.1016\/j.cropro.2019.105014","article-title":"Multiple Detoxification Genes Confer Imidacloprid Resistance to Sitobion avenae Fabricius","volume":"128","author":"Zhang","year":"2020","journal-title":"Crop Prot."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Yang, Y.X., Lin, R.H., Li, Z., Wang, A.Y., Xue, C., Duan, A.L., Zhao, M., and Zhang, J.H. (2021). Function Analysis of P450 and GST Genes to Imidacloprid in Aphis craccivora (Koch). Front. Physiol., 11.","DOI":"10.3389\/fphys.2020.624287"},{"key":"ref_21","first-page":"2291","article-title":"Functional Characterization of CYP6QE1 and CYP6FV21 in Resistance to \u03bb-Cyhalothrin and Imidacloprid in Bradysia odoriphaga","volume":"72","author":"Zhang","year":"2024","journal-title":"J. Agric. Food Chem."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"15403","DOI":"10.1021\/acs.jafc.0c05763","article-title":"Contribution of Glutathione S-Transferases to Imidacloprid Resistance in Nilaparvata lugens","volume":"68","author":"Yang","year":"2020","journal-title":"J. Agric. Food Chem."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Li, S., Zhang, A., Dou, N., Qu, Z., Guo, Y., Zhou, W., Wu, D., Lin, Z., Feng, M., and Cui, H. (2024). RNA Interference Reveals the Impacts of CYP6CY7 on Imidacloprid Resistance in Aphis glycines. Insects, 15.","DOI":"10.3390\/insects15030188"},{"key":"ref_24","first-page":"101630","article-title":"Investigating Imidacloprid Resistance in Amrasca biguttula biguttula (Ishida) (Hemiptera: Cicadellidae): Insights from RNA-Seq and Functional Validation Using RT-qPCR","volume":"56","author":"Mohan","year":"2025","journal-title":"Comp. Biochem. Physiol. Part D Genom. Proteom."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"2430","DOI":"10.1093\/jee\/toab196","article-title":"Sublethal Effects of Abamectin on the Development, Reproduction, Detoxification Enzyme Activity, and Related Gene Expression of the Oriental Fruit Moth (Lepidoptera: Tortricidae)","volume":"114","author":"Su","year":"2021","journal-title":"J. Econ. Entomol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"248","DOI":"10.1016\/0003-2697(76)90527-3","article-title":"A Rapid and Sensitive Method for the Quantitation of Microgram Quantities of Protein Utilizing the Principle of Protein-Dye Binding","volume":"72","author":"Bradford","year":"1976","journal-title":"Anal. Biochem."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"2809","DOI":"10.1002\/ps.5829","article-title":"Super-kdr Mutation M918L and Multiple Cytochrome P450s Associated with the Resistance of Rhopalosiphum padi to Pyrethroid","volume":"76","author":"Wang","year":"2020","journal-title":"Pest Manag. Sci."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"402","DOI":"10.1006\/meth.2001.1262","article-title":"Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2\u2212\u0394\u0394CT Method","volume":"25","author":"Livak","year":"2001","journal-title":"Methods"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"104725","DOI":"10.1016\/j.pestbp.2020.104725","article-title":"Characterization of Rhopalosiphum padi Takeout-Like Genes and Their Role in Insecticide Susceptibility","volume":"171","author":"Peng","year":"2021","journal-title":"Pestic. Biochem. Physiol."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Silva, A.X., Jander, G., Samaniego, H., Ramsey, J.S., and Figueroa, C.C. (2012). Insecticide Resistance Mechanisms in the Green Peach Aphid Myzus persicae (Hemiptera: Aphididae) I: A Transcriptomic Survey. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0036366"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1093\/bfgp\/elad019","article-title":"Quantifying Transcriptome Diversity: A Review","volume":"23","author":"Jones","year":"2024","journal-title":"Brief. Funct. Genom."},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Puinean, A.M., Foster, S.P., Oliphant, L., Denholm, I., Field, L.M., Millar, N.S., Williamson, M.S., and Bass, C. (2010). Amplification of a Cytochrome P450 Gene Is Associated with Resistance to Neonicotinoid Insecticides in the Aphid Myzus persicae. PLoS Genet., 6.","DOI":"10.1371\/journal.pgen.1000999"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1762","DOI":"10.1038\/s41598-017-01961-4","article-title":"Overexpression of a Cytochrome P450 and a UDP-Glycosyltransferase Is Associated with Imidacloprid Resistance in the Colorado Potato Beetle, Leptinotarsa decemlineata","volume":"7","author":"Kaplanoglu","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Antony, B., Johny, J., Abdelazim, M.M., Jak\u0161e, J., Al-Saleh, M.A., and Pain, A. (2019). Global Transcriptome Profiling and Functional Analysis Reveal That Tissue-Specific Constitutive Overexpression of Cytochrome P450s Confers Tolerance to Imidacloprid in Palm Weevils in Date Palm Fields. BMC Genom., 20.","DOI":"10.1186\/s12864-019-5837-4"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"34992","DOI":"10.1038\/srep34992","article-title":"Functional Analysis of CYP6ER1, a P450 Gene Associated with Imidacloprid Resistance in Nilaparvata lugens","volume":"6","author":"Pang","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1016\/j.ibmb.2016.10.009","article-title":"Metabolic Imidacloprid Resistance in the Brown Planthopper, Nilaparvata lugens, Relies on Multiple P450 Enzymes","volume":"79","author":"Zhang","year":"2016","journal-title":"Insect Biochem. Mol. Biol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"127490","DOI":"10.1016\/j.chemosphere.2020.127490","article-title":"Adipokinetic Hormone Regulates Cytochrome P450-Mediated Imidacloprid Resistance in the Brown Planthopper, Nilaparvata lugens","volume":"259","author":"Tang","year":"2020","journal-title":"Chemosphere"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"105743","DOI":"10.1016\/j.pestbp.2023.105743","article-title":"The Role of the Bemisia tabaci and Trialeurodes vaporariorum Cytochrome-P450 Clade CYP6DPx in Resistance to Nicotine and Neonicotinoids","volume":"198","author":"Pym","year":"2024","journal-title":"Pestic. Biochem. Physiol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"105469","DOI":"10.1016\/j.pestbp.2023.105469","article-title":"Novel_miR-1517 Mediates CYP6CM1 to Regulate Imidacloprid Resistance in Bemisia tabaci (Hemiptera: Gennadius)","volume":"194","author":"Gong","year":"2023","journal-title":"Pestic. Biochem. Physiol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"103934","DOI":"10.1016\/j.ibmb.2023.103934","article-title":"A Single Point Mutation in the Bemisia tabaci Cytochrome-P450 CYP6CM1 Causes Enhanced Resistance to Neonicotinoids","volume":"156","author":"Pym","year":"2023","journal-title":"Insect Biochem. Mol. Biol."},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Hu, J., Chen, F., Wang, J., Rao, W., Lin, L., and Fan, G.C. (2023). Multiple Insecticide Resistance and Associated Metabolic-Based Mechanisms in a Myzus persicae (Sulzer) Population. Agronomy, 13.","DOI":"10.3390\/agronomy13092276"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1141","DOI":"10.1007\/s10529-005-8464-x","article-title":"Expression and Characterization of Carboxylesterase E4 Gene from Peach-Potato Aphid (Myzus persicae) for Degradation of Carbaryl and Malathion","volume":"27","author":"Lan","year":"2005","journal-title":"Biotechnol. Lett."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"3390","DOI":"10.1021\/acs.jafc.9b06690","article-title":"Functional Characterization of Two Carboxylesterase Genes Involved in Pyrethroid Detoxification in Helicoverpa armigera","volume":"68","author":"Li","year":"2020","journal-title":"J. Agric. Food Chem."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"105443","DOI":"10.1016\/j.pestbp.2023.105443","article-title":"Identification, Expression Profiles and Involvement in Insecticides Tolerance and Detoxification of Carboxylesterase Genes in Bactrocera dorsalis","volume":"193","author":"Li","year":"2023","journal-title":"Pestic. Biochem. Physiol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"5713","DOI":"10.7150\/ijbs.77141","article-title":"Functional and Structural Diversity of Insect Glutathione S-Transferases in Xenobiotic Adaptation","volume":"18","author":"Moural","year":"2022","journal-title":"Int. J. Biol. Sci."},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Zhu, B., Li, L., Wei, R., Liang, P., and Gao, X. (2021). Regulation of GSTu1-Mediated Insecticide Resistance in Plutella xylostella by miRNA and lncRNA. PLoS Genet., 17.","DOI":"10.1371\/journal.pgen.1009888"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"1064","DOI":"10.1038\/s42003-023-05447-0","article-title":"Transcriptional Regulation and Overexpression of GST Cluster Enhances Pesticide Resistance in the Cotton Bollworm, Helicoverpa armigera (Lepidoptera: Noctuidae)","volume":"6","author":"Jin","year":"2023","journal-title":"Commun. Biol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1016\/j.pestbp.2017.03.007","article-title":"Cross-resistance pattern and basis of resistance in a thiamethoxam-resistant strain of Aphis gossypii Glover","volume":"138","author":"Wei","year":"2017","journal-title":"Pestic. Biochem. Physiol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1016\/j.pestbp.2014.12.002","article-title":"Elevated expression of esterase and cytochrome P450 are related with lambda-cyhalothrin resistance and lead to cross resistance in Aphis glycines Matsumura","volume":"118","author":"Xi","year":"2015","journal-title":"Pestic. Biochem. Physiol."}],"container-title":["Insects"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2075-4450\/17\/9\/973\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,9,23]],"date-time":"2026-09-23T04:20:08Z","timestamp":1790137208000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2075-4450\/17\/9\/973"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,9,21]]},"references-count":49,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2026,9]]}},"alternative-id":["insects17090973"],"URL":"https:\/\/doi.org\/10.3390\/insects17090973","relation":{},"ISSN":["2075-4450"],"issn-type":[{"value":"2075-4450","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,9,21]]}}}