Field efficacy of the pupal parasitoid Chouioia cunea Yang, 1989 (Hymenoptera: Eulophidae) and selected insecticides for management of Hyphantria cunea (Drury, 1773) (Lepidoptera: Erebidae) in hazelnut orchards

Öz

The fall webworm, Hyphantria cunea (Drury, 1773) (Lepidoptera: Erebidae), is a destructive polyphagous pest that poses a serious threat to hazelnut production worldwide. Effective management strategies are critical for minimizing its economic impact. This study aimed to evaluate the field efficacy of the pupal parasitoid Chouioia cunea Yang, 1989 (Hymenoptera: Eulophidae) and three insecticides ‒Bacillus thuringiensis var. kurstaki, azadirachtin, and diflubenzuron‒ applied in hazelnut orchards in Düzce province of Türkiye, between 2020 and 2021. To evaluate their distinct life-stage efficacies, larval mortality was assessed using a randomized complete block design following insecticide treatments targeting early instars, and pupal parasitism was assessed using a randomized plots design across two generations following parasitoid releases. Releases of C. cunea significantly increased pupal parasitism rates, reaching 86.06% in 2020 and 94.95% in 2021, compared to those in the untreated control plots. All insecticide treatments significantly suppressed larval populations, with B. thuringiensis and diflubenzuron consistently achieving higher efficacy than azadirachtin. In 2020, these two insecticides achieved efficacy levels exceeding 77%, while azadirachtin remained below 68%. In 2021, all insecticides showed improved performance, surpassing 90%, although azadirachtin remained slightly less effective. These findings support the potential of utilizing both biological control agents and selective insecticides as complementary tools within a sustainable and environmentally friendly strategy for managing H. cunea in hazelnut orchards.

Anahtar Kelimeler

• Azadirachtin
• Bacillus thuringiensis var. kurstaki
• diflubenzuron
• fall webworm
• inundative release

Destekleyen Kurum

This study was supported by the Scientific and Technological Research Council of Türkiye TUBITAK, Türkiye, Grant Project No: 118O529

Proje Numarası

TÜBİTAK, Proje No: 118O529

Teşekkür

The authors extend their gratitude to the Scientific and Technological Research Council of Türkiye (TUBITAK) Project No: 118O529) for funding this research.

Fındık bahçelerinde Hyphantria cunea (Drury, 1773) (Lepidoptera: Erebidae) ile mücadelede pupa parazitoidi Chouioia cunea Yang, 1989 (Hymenoptera: Eulophidae) ve bazı insektisitlerin etkinliği

Öz

Amerikan beyazkelebeği, Hyphantria cunea (Drury, 1773) (Lepidoptera: Erebidae), dünya genelinde fındık üretimi için ciddi bir tehdit oluşturan tahripkâr ve polifag bir zararlıdır. Bu zararlının ekonomik zararını en aza indirmek için etkili mücadele stratejileri büyük önem taşımaktadır. Bu çalışma; pupa parazitoidi Chouioia cunea Yang, 1989 (Hymenoptera: Eulophidae) ile üç farklı insektisitin (Bacillus thuringiensis var. kurstaki, azadiraktin ve diflubenzuron) Düzce ilindeki fındık bahçelerinde, iki yıl boyunca arazi etkinliğini değerlendirmeyi amaçlamıştır. Uygulamaların, zararlının farklı yaşam dönemlerine olan etkilerini belirlemek amacıyla, erken dönem larvaları hedefleyen insektisit uygulamalarının ardından larva ölümleri tesadüf blokları deneme desenine göre, parazitoid salımlarının ardından ise pupa parazitlenmesi iki döl boyunca tesadüf parselleri deneme desenine göre değerlendirilmiştir. C. cunea salımları, kontrol parsellerine kıyasla pupa parazitlenme oranlarını önemli ölçüde artırarak 2020 yılında %86,06’ya, 2021 yılında ise %94,95’e ulaştırmıştır. Tüm insektisit uygulamaları larva popülasyonlarını önemli ölçüde baskı altına almış; B. thuringiensis ve diflubenzuron, azadiraktine göre tutarlı bir şekilde daha yüksek etkinlik göstermiştir. 2020 yılında bu iki insektisit %77’yi aşan etkinlik seviyelerine ulaşırken, azadiraktin %68’in altında kalmıştır. 2021 yılında tüm insektisitlerin etkinlik oranlarında bir artış gözlenerek %90’lara ulaşmış olup, buna karşılık azadiraktin, diğer uygulamalara kıyasla nispeten daha düşük bir etkinlik sergilemiştir. Bu bulgular, fındık bahçelerinde H. cunea ile mücadelede sürdürülebilir ve çevre dostu bir strateji kapsamında hem biyolojik mücadele etmenlerinin hem de bazı seçilmiş insektisitlerin birbirini tamamlayıcı bileşenler olarak kullanılma potansiyelini desteklemektedir.

Anahtar Kelimeler

• Azadiraktin
• Bacillus thuringiensis var. kurstaki
• diflubenzuron
• Amerikan beyazkelebeği
• kitlesel salım

Destekleyen Kurum

This study was supported by the Scientific and Technological Research Council of Türkiye TUBITAK, Türkiye, Grant Project No: 118O529

Proje Numarası

TÜBİTAK, Proje No: 118O529

Teşekkür

The authors extend their gratitude to the Scientific and Technological Research Council of Türkiye (TUBITAK) Project No: 118O529) for funding this research.

Kaynakça

1. Amirmohammadi, F., J. J. Sendi & A. Zibaee, 2012. Biomonitoring of the genotoxic and oxidative the effect of neemon mortality and physiological indices of Hyphantria cunea (Drury)(Lepidoptera). Munis Entomology & Zoology, 7 (1): 489-495.
2. Aygün, A. & B. Gülcü, 2020. Evaluation of spinosad and different Bacillus thuringiensis (Bacillaceae) strains against the larvae of Hyphantria cunea (Lepidoptera: Erebidae). Düzce University Journal of Science and Technology, 8 (4): 2289-2295. https://doi.org/10.29130/dubited.768800
3. Bayram, M. S., G. Kaçar, L. Rossini & N. Baser, 2025. Developmental thresholds and thermal requirements of two pupal parasitoids of the invasive fall webworm. Insects, 16 (3): 284 (1-13). https://doi.org/10.3390/insects16030284
4. Canhilal, R., 2011. Comparison of the virulence of Heterorhabdit nematodes on Galleria mellonella L. (Lepidoptera: Pyralidae). Journal of Agriculture Faculty of Gaziosmanpasa University, 28 (2): 43-52.
5. Chailleux, A., E. K. Mohl, M. Teixeira Alves, G. J. Messelink & N. Desneux, 2014. Natural enemy-mediated indirect interactions among prey species: potential for enhancing biocontrol services in agroecosystems. Pest Management Science, 70 (12): 1769-1779.
6. Chen, H., D. Hao, C. Chen, Y. Sun & X. Yu, 2023. Effects of midgut bacteria in Hyphantria cunea (Lepidoptera: Erebidae) on nuclear polyhedrosis virus and Bacillus thuringiensis (Bacillales: Bacillaceae). Journal of Insect Science, 23 (2): 1 (1-9). https://doi.org/10.1093/jisesa/iead009
7. Chen, Q., H. Zhao, M. Wen, J. Li, H. Zhou, J. Wang & Y. Wang, 2020. Genome of the webworm Hyphantria cunea unveils genetic adaptations supporting its rapid invasion and spread. BMC Genomics, 21 (1): 242 (1-22).
8. Choi, W. I. & Y. S. Park, 2012. Dispersal patterns of exotic forest pests in South Korea. Insect Science, 19 (5): 535-548.

9. Dreistadt, S. H., 2014. Biological Control and Natural Enemies of Invertebrates: Integrated Pest Management for Home Gardeners and Landscape Professionals. University of California, Davis, Agriculture and Natural Resources, California, 6 pp.
10. Edosa, T. T., Y. H. Jo, M. Keshavarz, Y. S. Anh, M. Y. Noh & Y. S. Han, 2019. Current status of the management of fall webworm, Hyphantria cunea: towards the integrated pest management development. Journal of Applied Entomology, 143 (1-2): 1-10.
11. FAOStat, 2024. Statistics of crops and livestock products. (Web page: https://www.fao.org/faostat/en/#data/QCL) (Date accessed: December 2024).
12. Ge, X., S. He, C. Zhu, T. Wang, Z. Xu & S. Zong, 2019. Projecting the current and future potential global distribution of Hyphantria cunea (Lepidoptera: Arctiidae) using CLIMEX. Pest Management Science, 75 (1): 160-169.
13. Giovanni, G. D., G. Oliva, & A. Montermini, 1986. Defence strategy against the American Hyphantria. Informatore Fitopatologico, 36 (2): 11-15.
14. Güler, E. & F. Balta, 2020. Determination of yield and quality characteristics of hazelnut populations of Taskesti district (Mudurnu-Bolu). International Journal of Agriculture and Wildlife Science, 6 (2): 115-128. (in Turkish with abstract in English) https://doi.org/10.24180/ijaws.685813
15. Han, G. S., J. G. Wang, W. He, H. K. Wang, A. L. Chen & X. Q. Yang, 2000. Artificial propagation of Chouioia cunea and its applied technology. Forest Pest and Disease, 19 (1): 26-28. https://doi.org/10.3969/j.issn.1671-0886.2000.01.009
16. Isin, M., K. I. Shanimov & B. Kopzhasarov, 2008. American fall webworm in Kazakhstan. Zashchita i Karantin Rasteniĭ, 9: 39.
17. Japoshvili, G., A. Nikolaisiivili, N. Dzneladze & L. Goguadze, 2006. The fall webworm (Hyphantria cunea) in western Georgia. Proceedings of the Georgian Academy of Sciences, Biological Series B, 4 (4): 122-126.
18. Kaçar, G. & A. S. Koca, 2025a. Release of Psychophagus omnivorus (Walker, 1835) (Hymenoptera: Pteromalidae) against Hyphantria cunea (Drury, 1773) (Lepidoptera: Erebidae) in hazelnut orchards. Turkish Journal of Entomology, 49 (4): 379-388. https://doi.org/10.16970/entoted.1758801
19. Kaçar, G. & A. S. Koca, 2025b. Düzce ilinde Amerikan beyazkelebeği Hyphantria cunea (Drury) (Lepidoptera: Erebidae)’nın pupa parazitoitleri ile parazitlenme oranları. Turkish Journal of Biological Control, 16 (2): 24-36. (in Turkish with abstract in English) https://doi.org/10.31019/tbmd.1727722
20. Kaçar, G., A. Butrón, D. Kontogiannatos, P. Han, M. G. F. V. Peñaflor, G. P. Farinós, F. Huang, W. D. Hutchison, B. H. S. de Souza, R. A. Malvar, A. Kourti, R. Ramirez-Romero, J. L. Smith, A. S. Koca, M. Pineda & K. Haddi, 2023. Recent trends in management strategies for İtwo major maize borers: Ostrinia nubilalis and Sesamia nonagrioides. Journal of Pest Science, 96 (3): 879-901. https://doi.org/10.1007/s10340-023-01595-8
21. Kaçar, G., A. S. Koca, B. Şahin & F. Yıldız, 2019. The distribution area, damage rate and some bio-ecological characters of American the fall webworm in hazelnut orchards in Bolu and Düzce. International Journal of Agriculture and Wildlife Science, 5 (2): 266-272. (in Turkish with abstract in English) https://doi.org/10.24180/ijaws.563804
22. Kaçar, G., A. S. Koca, H. Kütük & B. Şahin, 2017. “Natural parasitism rate of the fall webworm in hazelnut groves in Düzce, 71”. 2nd International Iğdır Symposium (9-11 October 2017, Iğdır), 444 s. (in Turkish with abstract in English)
23. Kaçar, G., A. S. Koca, M. S. Bayram & B. Şahin, 2022. Population dynamics of the fall webworm, Hyphantria cunea Drury (Lepidoptera: Erebidae) in hazelnut orchards of Düzce province. Turkish Journal of Agricultural and Natural Sciences, 9 (1): 77-84. (in Turkish with abstract in English) https://doi.org/10.30910/turkjans.953289
24. Karami, A., A. Talebi, E. Gilasian, Y. Fathipour & M. Mehrabadi, 2023. Native parasitoids of the fall webworm, Hyphantria cunea (Drury, 1773) (Lepidoptera, Erebidae), an invasive alien pest in northern Iran. Journal of Insect Biodiversity and Systematics, 9 (1): 81-101. https://doi.org/10.52547/jibs.9.1.81
25. Kiyota, R., M. Arakawa, R. Yamakawa, A. Yasmin & T. Ando, 2011. Biosynthetic pathways of the sex pheromone components and substrate selectivity of the oxidation enzymes working in pheromone glands of the fall webworm, Hyphantria cunea. Insect Biochemistry and Molecular Biology, 41 (6): 362-369.
26. Li, T., X. Wang, N. Desneux, L. Song & L. Zang, 2022. Performance of Chouioia cunea reared from a coleopteran alternative host as a biocontrol agent against the invasive lepidopteran pest, Hyphantria cunea. Pest Management Science, 79 (4): 1500-1507. https://doi.org/10.1002/ps.7318
27. Montermini, A. & G. Oliva, 1984. Let us learn to know the fall webworm. Informatore Fitopatologico, 34 (1): 35-40.
28. Palacios-Cortez, L., F. Gandarilla-Pacheco, L. Morales-Ramos, S. Salcedo-Martínez, M. Alemán-Huerta, M. Elías Santos & I. Quintero-Zapata, 2022. Roencapsulación de Bacillus thuringiensis (Berliner) en matrices biopoliméricas con secado por aspersión para el control de Hyphantria cunea (Drury). Tropical and Subtropical Agroecosystems, 25 (2): 60 (1-11). (in Spanish with abstract in English) https://doi.org/10.56369/tsaes.4156
29. Pan, L., W. Gao, X. Liu, D. Qin, T. Zhang, R. Ren & M. Li, 2023. Parasitoids as taxonomists: how does the parasitoid Chouioia cunea distinguish between a host and a non‐host? Pest Management Science, 79 (11): 4547-4556. https://doi.org/10.1002/ps.7656
30. Pereira, M. F. & C. C. Rossi, 2020. Overview of rearing and testing conditions and a guide for optimizing Galleria mellonella breeding and use in the laboratory for scientific purposes. Apmis, 128 (12): 607-620.
31. Qu, B. X., H. H. Li, X. Y. Ao, X. L. Ren, B. M. Guo & W. P. Wang, 1987. Forecasting study of Hyphantria cunea. Journal of Northwest College of Forestry, 2 (2): 41-49.
32. R Core Team, 2016. R: a language and environment for statistical computing. Vienna, Austria: R foundation for statistical computing. (Web page: https://www.R-project.org/) (Date accessed: April 2026)
33. Rezaei, V., S. Moharramipour, Y. Fathipour & A. A. Talebi, 2006. Nutritional indices and host preference of American white webworm, Hyphantria cunea (Lepidoptera: Arctiidae) on five host plants. Journal of Entomological Society of Iran, 26 (1): 57-72.
34. Saruhan, I., I. Akca & R. Kushiyev (2014). Toxicity of some biopesticides to the fall webworm, Hyphantria cunea Durry (Lepidoptera: Arctidae). Egyptian Journal of Biological Pest Control, 24 (1): 255-257.
35. Schowalter, T. D. & D. R. Ring, 2017. Biology and management of the fall webworm, Hyphantria cunea (Lepidoptera: Erebidae). Journal of Integrated Pest Management, 8 (1): 7 (1-6).
36. Su, Z. S., Z. Q. Yang, J. R. Wei & X. Y. Wang, 2004. Studies on alternate hosts of the parasitoid Chouioia cunea (Hymenoptera: Eulophidae). Scientia Silvae Sinicae, 40 (4): 106-116.
37. Sun, H. Y., B. Cong, H.Y. Zhang, H. Dong & L. Cui, 2010. Relationship between female fecundity, developing time and female body size of Chouioia cunea Yang (Hymenoptera: Eulophidae). Chinese Journal of Biological Control, 26 (1): 24-29.
38. Tuncer, C. & İ. A. Kansu, 1994. Studies on the effects of the some host plants on the fall webworm (Hyphantria cunea (Drury), Lepidoptera, Arctiidae). Turkish Journal of Entomology, 18 (4): 209-222. (in Turkish with abstract in English)
39. Wu, N., S. Zhang, X. Li, Y. Cao, X. Liu, Q. Wang & S. Zhan, 2019. Fall webworm genomes yield insights into rapid adaptation of invasive species. Nature Ecology and Evolution, 3 (1): 105-115.
40. Yang, Z. Q. & E. K. Xie, 1998. Behavior of Chouioia cunea Yang (Hymenoptera: Eulophidae). Chinese Journal of Biological Control, 14 (2): 49-52.
41. Yang, Z. Q., 1989. A new genus and species of Tetrastichinae (Hymenoptera: Eulophidae) parasitizing Hyphantria cunea in China. Entomotaxonomia, 11 (1-2): 117-130.
42. Yang, Z. Q., J. R. Wei & X. Y. Wang, 2006. Mass rearing and augmentative releases of the native parasitoid Chouioia cunea for biological control of the introduced fall webworm Hyphantria cunea in China. Biocontrol, 51 (4): 401-418.
43. Yang, Z. Q., X. Y. Wang & Y. N. Zhang, 2014. Recent advances in biological control of important native and invasive forest pests in China. Biological Control, 68 (2014): 117-128.
44. Yang, Z. Q., X. Y. Wang, C. Z. Wang, X. R. Qiao & J. J. Pang, 2005. Studies on utilizing parasitoid Chouioia cunea Yang (Hymenoptera: Eulophidae) for sustainable control of fall webworm. Scientia Silvae Sinicae, 41 (5): 72-80. https://doi.org/10.11707/j.1001-7488.20050512
45. Yang, Z. Q., X. Y. Wang, J. R. Wei, H. R. Qu & X. R. Qiao, 2008. Survey of the native insect natural enemies of Hyphantria cunea (Drury) (Lepidoptera: Arctiidae) in China. Bulletin of Entomological Research, 98 (3): 293-302.
46. Yang, Z. Y. & Y. Z. Zhang, 2007. Researches on techniques for biocontrol of the fall webworm, Hyphantria cunea, a severe invasive insect pest to China. Chinese Bulletin of Entomology, 44 (4): 465-471.
47. Zalucki, M. P., A. R. Clarke & S. B. Malcolm, 2002. Ecology and behavior of first instar larval Lepidoptera. Annual Review of Entomology, 47 (1): 361-393.
48. Zhang, Q. H., F. Schlyter, D. Chu, X. Y. Ma & Y. Ninomiya, 1996. Female calling behaviour and response of males to synthetic pheromone and virgin females in spring and summer generations of Hyphantria cunea (Lepidoptera: Arctiidae) in Northeastern China. Journal of Applied Entomology, 120 (1-5): 467-476.
49. Zhao, L. & W. Wang, 2021. Effects of autumn warming on energy consumption of diapausing fall webworm (Lepidoptera: Arctiidae) pupae. Journal of Insect Science, 21 (2): 8 (1-7). https://doi.org/10.1093/jisesa/ieab021
50. Zhao, L., X. Wang, Z. Liu & A. Torson, 2022. Energy consumption and cold hardiness of diapausing fall webworm pupae. Insects, 13 (9): 853 (1-11). https://doi.org/10.3390/insects13030853
51. Zhao, L., X. Xu, Z. Xu, Y. Liu & S. Sun, 2014. Diapause induction, color change, and cold tolerance physiology of the diapausing larvae of the Chouioia cunea (Hymenoptera: Eulophidae). Journal of Insect Science, 14 (1): 294 (1-5). https://doi.org/10.1093/jisesa/ieu156
52. Zhu, G., L. Pan, Y. Zhao, X. Zhang, F. Wang, Y. Yu & M. Li, 2016. Chemical investigations of volatile kairomones produced by Hyphantria cunea (Drury), a host of the parasitoid Chouioia cunea Yang. Bulletin of Entomological Research, 107 (2): 234-240. https://doi.org/10.1017/S0007485316000833