Identification and activity evaluation of the sex pheromone of Argyrogramma agnata Staudinger in China

Abstract

Studying the polymorphism of insect pheromones can inform effective local pest management strategies. The sex pheromones of Argyrogramma agnata Staudinger, a significant polyphagous migratory pest, have not been previously reported. In this study, two components, Z7-12:Ac and Z9-12:Ac, were identified from the gland extracts of A. agnata females using gas chromatography-electroantennographic detection and gas chromatography coupled with time-of-flight mass spectrometry. Males exhibited a strong electroantennographic response to both components with a clear dose–response relationship. Field trials demonstrated that males were effectively attracted to an 8:3 ratio of Z7-12:Ac and Z9-12:Ac at a dose of 1100 μg. Lures equipped with box traps captured significantly more males than those with uni traps, delta traps, or wing traps. These findings elucidate the sex pheromone components of the A. agnata population and optimize their field application, providing valuable guidance for the integrated pest management of A. agnata in China.

Keywords

Argyrogramma agnata Staudinger / integrated pest management / pheromone polymorphism / sex pheromone / trap screening

References

[1] Yew, J. Y., & Chung, H. (2015). Insect pheromones: An overview of function, form, and discovery. Progress in Lipid Research, 59, 88-105. https://doi.org/10.1016/j.plipres.2015.06.001

[2] Cusumano, A., Harvey, J. A., Bourne, M. E., Poelman, E. H., & G de Boer, J. (2020). Exploiting chemical ecology to manage hyperparasitoids in biological control of arthropod pests. Pest Management Science, 76(2), 432-443. https://doi.org/10.1002/ps.5679

[3] Wang, A. J., Zhang, K. X., Gao, Y. L., Weng, A. Z., Wang, L. Y., Zhang, Y. H., Zhang, Z., She, D. M., Ning, J., & Mei, X. D. (2019). Synthesis and bioactivity studies of sex pheromone analogs of the diamond back moth, Plutella xylostella. Pest Management Science, 75(4), 1045-1055. https://doi.org/10.1002/ps.5214

[4] Xu, L., Xie, Y., Na, R., & Li, Q. X. (2020). Mini-review: Recent advances in the identification and application of sex pheromones of gall midges (Diptera: Cecidomyiidae). Pest Management Science, 76(12), 3905-3910. https://doi.org/10.1002/ps.5949

[5] Butenandt, A., Beckmann, R., Stammu, D., Hecker, E., & Naturforsch, Z. (1959). Uber den sexsual-lockstoff des seidenspinners Bombyx mori. Zeitschrift für Naturforschung, 14b, 283-284.

[6] Ando, T., & Yamamoto, M. (2020). Semiochemicals containing lepidopteran sex pheromones: Wonderland for a natural product chemist. Journal of Pesticide Science, 45(4), 191-205. https://doi.org/10.1584/jpestics.D20-046

[7] Bontonou, G., Denis, B., & Wicker-Thomas, C. (2012). Male pheromone polymorphism and reproductive isolation in populations of Drosophila simulans. Ecology and Evolution, 2(10), 2527-2536. https://doi.org/10.1002/ece3.342

[8] Cardé, R. T. (1986). The role of pheromones in reproductive isolation and speciation of insects. In M. D. Huettel (Ed.), Evolutionary Genetics of Invertebrate Behavior (pp. 303-317). Springer. https://doi.org/10.1007/978-1-4899-3487-1_29

[9] De Pasqual, C., Selenius, E., Burdfield-Steel, E., & Mappes, J. (2024). Morph-linked variation in female pheromone signaling and male response in a polymorphic moth. Journal of Animal Ecology, 93(11), 1697-1709. https://doi.org/10.1111/1365-2656.14182

[10] Wang, C., Zhang, S., Guo, M. B., Hou, X. Q., Yang, B., & Wang, G. R. (2022). Optimization of a pheromone lure by analyzing the peripheral coding of sex pheromones of Spodoptera frugiperda in China. Pest Management Science, 78(7), 2995-3004. https://doi.org/10.1002/ps.6924

[11] Wakamura, S., Arakaki, N., & Yoshimatsu, S. (2021). Sex pheromone of the fall armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae) of a “far east” population from Okinawa, Japan. Applied Entomology and Zoology, 56(1), 19-25. https://doi.org/10.1007/s13355-020-00703-9

[12] Li, C., Fu, X., Feng, H., Ali, A., Li, C., & Wu, K. (2014). Seasonal migration of Ctenoplusia agnata (Lepidoptera: Noctuidae) over the Bohai sea in northern China. Journal of Economic Entomology, 107(3), 1003-1008. https://doi.org/10.1603/ec13534

[13] Park, K. T., Hwang, C., & Choi, K. M. (1978). Lepidopterous insect pests on soybean. Journal of Plant Protection, 17(1), 1-5.

[14] Umetsu, Y., & Nagano, T. (1998). The outbreak of Acanthoplusia agnata (Staudinger) in soybean fields, in Miyagi Prefecture. Annual Report of the Society of Plant Protection of North Japan, 49, 153-155. https://doi.org/10.11455/kitanihon1966.1998.153

[15] Yu, Y., Shi, S., Xu, M., & Cui, J. (2018). Current research on soybean pest management in China. Oil Crop Science, 3(4), 215-227. https://doi.org/10.3969/j.issn.2096-2428.2018.04.002

[16] Zhang, Z., Li, Y., Li, J., & Guo, X. (2016). The prevention and control technology of Argyrogramma agnata Staudinger. Agricultural Technology Service, 33(4), 20-21. https://doi.org/10.3969/j.issn.1004-8421.2016.04.007

[17] Horowitz, A. R., Ellsworth, P. C., & Ishaaya, I. (2009). Biorational pest control–an overview. In I. Ishaaya & A. Horowitz (Eds.), Biorational Control of Arthropod Pests (pp. 1-20). Springer. https://doi.org/10.1007/978-90-481-2316-2_1

[18] Khan, M. A., Khan, Z., Ahmad, W., Paul, B., Paul, S., Aggarwal, C., & Akhtar, M. S. (2015). Insect pest resistance: An alternative approach for crop protection. In K. Hakeem (Ed.), Crop Production and Global Environmental Issues (pp. 257-282). Springer. https://doi.org/10.1007/978-3-319-23162-4_11

[19] Witzgall, P., Kirsch, P., & Cork, A. (2010). Sex pheromones and their impact on pest management. Journal of Chemical Ecology, 36(1), 80-100. https://doi.org/10.1007/s10886-009-9737-y

[20] Sugie, H., Kawasaki, K., Higuchi, H., Kitamura, C., & Tamaki, Y. (1990). Identification of the sex pheromone of the three-spotted plusia, Acanthoplusia agnata Staudinger (Lepidoptera: Noctuidae). Applied Entomology and Zoology, 25(4), 467-473. https://doi.org/10.1303/aez.25.467

[21] Van Hai, T., Van Vang, L., Son, P. K., Inomata, S., & Ando, T. (2002). Sex attractants for moths of Vietnam: Field attraction by synthetic lures baited with known lepidopteran pheromones. Journal of Chemical Ecology, 28(7), 1473-1481. https://doi.org/10.1023/a:1016208921583

[22] El-Sayed, A. M., Ganji, S., Gross, J., Giesen, N., Rid, M., Lo, P. L., Kokeny, A., & Unelius, C. R. (2021). Climate change risk to pheromone application in pest management. Science and Nature, 108(6), 47. https://doi.org/10.1007/s00114-021-01757-7

[23] Yan, J., Zhang, M., Ali, A., Du, X., Mei, X., & Gao, Y. (2022). Optimization and field evaluation of sex-pheromone of potato tuber moth, Phthorimaea operculella Zeller (Lepidoptera: Gelechiidae). Pest Management Science, 78(9), 3903-3911. https://doi.org/10.1002/ps.6725

[24] Kehat, M., Anshelevich, L., Dunkelblum, E., Fraishtat, P., & Greenberg, S. (1994). Sex pheromone traps for monitoring the codling moth: Effect of dispenser type, field aging of dispenser, pheromone dose and type of trap on male captures. Entomologia Experimentalis et Applicata, 70(1), 55-62. https://doi.org/10.1111/j.1570-7458.1994.tb01758.x

[25] Zhao, Z., Rong, E., Li, S., Zhang, L., Kong, W., Hu, R., Zhang, J., & Ma, R. (2013). Research on the practical parameters of sex pheromone traps for the oriental fruit moth. Pest Management Science, 69(10), 1181-1186. https://doi.org/10.1002/ps.3592

[26] Baker, T. C., Meyer, W., & Roelofs, W. L. (1981). Sex pheromone dosage and blend specificity of response by oriental fruit moth males. Entomologia Experimentalis et Applicata, 30(3), 269-279. https://doi.org/10.1111/j.1570-7458.1981.tb03110.x

[27] Rizvi, S. A. H., George, J., Reddy, G. V. P., Zeng, X., & Guerrero, A. (2021). Latest developments in insect sex pheromone research and its application in agricultural pest management. Insects, 12(6), 484. https://doi.org/10.3390/insects12060484

[28] Sun, D. (2011). Study on the control technique of Dendrotonus valens Leconte with the application of pheromone [Master’s thesis. Beijing Forestry University].

[29] Witzgall, P., Bengtsson, M., & Trimble, R. M. (2000). Sex pheromone of grape berry moth (lepidoptera: Tortricidae). Environmental Entomology, 29(3), 433-436. https://doi.org/10.1603/0046-225x-29.3.433

[30] Deng, J. Y., Lan, C. Y. H., Zhou, J. X., Yao, Y. B., Yin, X. H., Fu, K. Y., Ding, X. H., Guo, W. C., Liu, W., Wang, N., & Wang, F. (2023). Analysis of sex pheromone production and field trapping of the Asian corn borer (Ostrinia furnacalis Guenée) in Xinjiang, China. Journal of Integrative Agriculture, 22(4), 1093-1103. https://doi.org/10.1016/j.jia.2022.08.042

[31] Buser, H. R., Arn, H., Guerin, P., & Rauscher, S. (1983). Determination of double bond position in mono-unsaturated acetates by mass spectrometry of dimethyl disulfide adducts. Analytical Chemistry, 55(6), 818-822. https://doi.org/10.1021/ac00257a003

[32] Syed, Z., & Leal, W. S. (2011). Electrophysiological measurements from a moth olfactory system. Journal of Visualized Experiments, 49, e2489. https://doi.org/10.3791/2489

[33] Wang, L., Mei, X., Zhang, Z., Weng, A., Ma, H., She, D., Ning, J., Xie, A., & Mu, C. (2020). Synthesis and preliminary activities of novel sex pheromone analogs of Macdunnoughia crassisigna Warren. Chinese Journal of Synthetic Chemistry, 28(6), 477-482. https://doi.org/10.15952/j.cnki.cjsc.1005-1511.19025

[34] Yan, Q., Zheng, M. Y., Xu, J. W., Ma, J. F., Chen, Y., Dong, Z. P., Liu, L., Dong, S. L., & Zhang, Y. N. (2018). Female sex pheromone of Athetis lepigone (Lepidoptera: Noctuidae): Identification and field evaluation. Journal of Applied Entomology, 142(1-2), 125-130. https://doi.org/10.1111/jen.12413

[35] Ando, T., & Yamakawa, R. (2011). Analyses of lepidopteran sex pheromones by mass spectrometry. TrAC, Trends in Analytical Chemistry, 30(7), 990-1002. https://doi.org/10.1016/j.trac.2011.03.010

[36] Honda, H., Yamasaki, R., Sumiuchi, Y., Uehara, T., Matsuyama, S., Ando, T., & Naka, H. (2015). Hybrid sex pheromones of the hibiscus flower-bud borer, Rehimena surusalis. Journal of Chemical Ecology, 41(11), 1043-1049. https://doi.org/10.1007/s10886-015-0638-y

[37] Inomata, S. I., Watanabe, A., Nomura, M., & Ando, T. (2005). Mating communication systems of four Plusiinae species distributed in Japan: Identification of the sex pheromones and field evaluation. Journal of Chemical Ecology, 31(6), 1429-1442. https://doi.org/10.1007/s10886-005-5295-0

[38] Jiang, Y., Ma, J., Wei, Y., Liu, Y., Zhou, Z., Huang, Y., Wang, P., & Yan, X. (2021). De novo biosynthesis of sex pheromone components of Helicoverpa armigera through an artificial pathway in yeast. Green Chemistry, 24(2), 767-778. https://doi.org/10.1039/D1GC02965G

[39] Tillman, J. A., Seybold, S. J., Jurenka, R. A., & Blomquist, G. J. (1999). Insect pheromones—An overview of biosynthesis and endocrine regulation. Insect Biochemistry and Molecular Biology, 29(6), 481-514. https://doi.org/10.1016/S0965-1748(99)00016-8

[40] Liedvogel, M., Åkesson, S., & Bensch, S. (2011). The genetics of migration on the move. Trends in Ecology and Evolution, 26(11), 561-569. https://doi.org/10.1016/j.tree.2011.07.009

[41] Buchinger, T. J., & Li, W. (2020). The evolution of (non)species-specific pheromones. Evolutionary Ecology, 34(4), 455-468. https://doi.org/10.1007/s10682-020-10046-0

[42] Racevska, E. (2018). Natural selection. In J. Vonk & T. Shackelford (Eds.), Encyclopedia of animal cognition and behavior (pp. 1-14). Springer International Publishing. https://doi.org/10.1007/978-3-319-47829-6_542-1

[43] Darwin, C. (2009). The descent of man and selection in relation to sex. Cambridge University Press. https://doi.org/10.1017/CBO9780511703829

[44] Fine, P. V. A. (2015). Ecological and evolutionary drivers of geographic variation in species diversity. Annual Review of Ecology, Evolution, and Systematics, 46(1), 369-392. https://doi.org/10.1146/annurev-ecolsys-112414-054102

[45] Wright, A. F. (2005). Genetic variation: Polymorphisms and mutations. Encyclopedia of Life Sciences. https://doi.org/10.1038/npg.els.0005005

[46] Jiang, N. J., Tang, R., Wu, H., Xu, M., Ning, C., Huang, L. Q., & Wang, C. Z. (2019). Dissecting sex pheromone communication of Mythimna separata (Walker) in North China from receptor molecules and antennal lobes to behavior. Insect Biochemistry and Molecular Biology, 111, 103176. https://doi.org/10.1016/j.ibmb.2019.103176

[47] Dong, S., & Du, J. (2002). Chemical identification and field tests of sex pheromone of beet armyworm Spodoptera exigua. Acta Phytophylacica Sinica, 29(1), 19-24. https://doi.org/10.13802/j.cnki.zwbhxb.2002.01.004

[48] Dillon, M. E., & Lozier, J. D. (2019). Adaptation to the abiotic environment in insects: The influence of variability on ecophysiology and evolutionary genomics. Current Opinion in Insect Science, 36, 131-139. https://doi.org/10.1016/j.cois.2019.09.003

[49] Baker, T. C., & Roelofs, W. L. (1981). Initiation and termination of oriental fruit moth male response to pheromone concentrations in the field. Environmental Entomology, 10(2), 211-218. https://doi.org/10.1093/ee/10.2.211

[50] Sisay, B., Subramanian, S., Weldon, C. W., Krüger, K., Khamis, F., Tefera, T., Torto, B., & Tamiru, A. (2024). Evaluation of pheromone lures, trap designs and placement heights for monitoring the fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae) in maize fields of Kenya. Crop Protection, 176, 106523. https://doi.org/10.1016/j.cropro.2023.106523

RIGHTS & PERMISSIONS

2025 The Author(s). New Plant Protection published by John Wiley & Sons Australia, Ltd on behalf of Institute of Plant Protection, Chinese Academy of Agricultural Sciences.