Effect of afidopyropen on the functional response and associated parameters of Trichogramma evanescens

Abstract

Afidopyropen, with a unique mode of action that modulates the chordotonal organ transient receptor potential vanilloid (TRPV) channel, serves as a promising insecticide against sap-sucking pests, particularly aphids. However, when targeting aphids, afidopyropen can affect non-target organisms such as Trichogramma species inhabiting the same habitats. The information regarding the effects of afidopyropen on Trichogramma species is limited, and there is an urgent need to expand our knowledge in this area. This study investigated the effects of afidopyropen treatment on the type of functional response and associated parameters, such as attack coefficient and handling time, of Trichogramma evanescens Westwood (Hymenoptera: Trichogrammatidae) females treated at the pupal stage. The findings clearly revealed that afidopyropen treatment did not change the type of functional response since both afidopyropen and control-treated parasitoids exhibited a type III functional response. Afidopyropen treatments did not affect the host handling time of the parasitoid either. However, the parasitoids treated with afidopyropen had a lower attack coefficient compared to the control group. The findings of this study suggest that afidopyropen does not alter the host handling strategy of T. evanescens, although it impaired the attack coefficient and may pose a threat to the natural effectiveness of the parasitoid. This current study highlights the requirement of further investigations aimed at determining the effects of afidopyropen on non-target insects.

Keywords

• Attack coefficient
• Natural enemies
• Novel insecticide
• Parasitism
• TRPV channel

References

1. Achiri TD, Fursov V, Atakan E, Pehlivan S (2020) First record and parasitism of egg parasitoid Trichogramma evanescens Westwood, 1833 (Hymenoptera: Trichogrammatidae) on eggs of Chilo partellus Swinhoe, 1885 (Lepidoptera: Crambidae) in Turkey. Turkish Journal of Entomology 44: 49-56. doi: 10.16970/entoted.590559.
2. Agamy E (2010) Field evaluation of the egg parasitoid, Trichogramma evanescens West. against the olive moth Prays oleae (Bern.) in Egypt. Journal of Pest Science 83: 53-58. doi: 10.1007/s10340-009-0273-x.
3. Bolker BM, R Development Core Team, Giné-Vázquez I (2023) bbmle (v1.0.25.1): Tools for general maximum likelihood estimation. An R Package.
4. Cônsoli FL, Botelho PSM, Parra JRP (2008) Selectivity of insecticides to the egg parasitoid Trichogramma galloi Zucchi, 1988, (Hym., Trichogrammatidae). Journal of Applied Entomology 125: 37-43. doi: 10.1111/j.1439-0418.2001.00513.x.
5. Fuchsberg JR, Yong TH, Losey JE, Carter ME, Hoffmann MP (2007) Evaluation of corn leaf aphid (Rhopalosiphum maidis; Homoptera: Aphididae) honeydew as a food source for the egg parasitoid Trichogramma ostriniae (Hymenoptera: Trichogrammatidae). Biological Control 40: 230-236. doi: 10.1016/j.biocontrol.2006.10.009.
6. GDFC (2022) Plant Protection Products Database. Turkish Ministry of Agriculture and Forestry. https://bku.tarimorman.gov.tr/ Accessed 30 September, 2024.
7. Hassell MP, Lawton JH, Beddington JR (1977) Sigmoid functional responses by invertebrate predators and parasitoids. Journal of Animal Ecology. 46: 249-262. doi: 10.2307/3959.
8. Horikoshi R, Goto K, Mitomi M, Oyama K, Hirose T, Sunazuka T, Ōmura S (2022) Afidopyropen, a novel insecticide originating from microbial secondary extracts. Scientific Reports 12: 2827. doi: 10.1038/s41598-022-06729-z.

9. Joseph SV (2020) Effect of afidopyropen against Myzus persicae (Hemiptera: Aphididae) and its predator, Adalia bipunctata (L.) in a greenhouse. Journal of Entomological Science 55: 584-587. doi: 10.18474/0749-8004-55.4.584.
10. Juliano SA (2001) Nonlinear curve fitting: Predation and functional response. In: Scheiner MS, Gurevitch J (Eds), Design and Analysis of Ecological Experiments. Oxford University Press. Inc., New York, USA. pp. 178-196.
11. Kandasamy R, London D, Stam L, von Deyn W, Zhao X, Salgado VL, Nesterov A (2017) Afidopyropen: New and potent modulator of insect transient receptor potential channels. Insect Biochemistry and Molecular Biology 84: 32-39. doi: 10.1016/j.ibmb.2017.03.005.
12. Katsuta H, Nomura M, Wakita T, Daido H, Kobayashi Y, Kawahara A, Banba S (2019) Discovery of broflanilide, a novel insecticide. Journal of Pesticide Science 44: 120-128. doi: 10.1584/jpestics.D18-088.
13. Klomp H, Teerink BJ, Ma WC (1980) Discrimination between parasitized and unparasitized hosts in the egg parasite Trichogramma embryophagum (Hym.: Trichogrammatidae): a matter of learning and forgetting. Netherlands Journal of Zoology 30: 254-277.
14. Koch RL, da Silva Queiroz O, Aita RC, Hodgson EW, Potter BD, Nyoike T, Ellers‐Kirk CD (2020) Efficacy of afidopyropen against soybean aphid (Hemiptera: Aphididae) and toxicity to natural enemies. Pest Management Science 76: 375-383. doi: 10.1002/ps.5525.
15. Lucchi A, Scaramozzino PL, Michl G, Loni A, Hoffmann C (2016) The first record in Italy of Trichogramma cordubense Vargas & Cabello 1985 (Hymenoptera trichogrammatidae) emerging from the eggs of Lobesia botrana (Denis & Schiffermüller, 1775) (Lepidoptera tortricidae). VITIS - Journal of Grapevine Research 55: 161–164. doi: 10.5073/vitis.2016.55.161-164.
16. Overton K, Ward SE, Hoffmann AA, Umina PA (2023) Lethal impacts of insecticides and miticides on three agriculturally important aphid parasitoids. Biological Control 178: 105143. doi: 10.1016/j.biocontrol.2022.105143.
17. Oztemiz S (2008) Natural parasitism rate of Trichogramma evanescens Westwood (Hymenoptera: Trichogrammatidae) and its release efficacy against the cotton bollworm, Helicoverpa armigera Hübner (Lepidoptera: Noctuidae) in the Cukurova region, Turkey. Entomological News 119: 19-33. doi: 10.3157/0013-872X(2008)119[19:NPROTE]2.0.CO;2.
18. Oztemiz S, Karacaoglu M, Yarpuzlu F (2009) Parasitization rate of Helicoverpa armigera Hübner (Lepidoptera: Noctuidae) eggs after field releases of Trichogramma evanescens Westwood (Hymenoptera: Trichogrammatidae) in cotton in Cukurova region of Turkey. Journal of the Kansas Entomological Society 82: 183-193. doi: 10.2317/JKES607.15.1.
19. Picanço MC, Bacci L, Crespo ALB, Miranda MMM, Martins JC (2007) Effect of integrated pest management practices on tomato production and conservation of natural enemies. Agricultural and Forest Entomology 9: 327-335. doi: 10.1111/j.1461-9563.2007.00346.x.
20. Polaszek A (2009) Species diversity and host associations of Trichogramma in Eurasia. In: Consoli F, Parra J, Zucchi R (eds) Egg Parasitoids in Agroecosystems with Emphasis on Trichogramma. Springer Netherlands, Dordrecht, pp. 237-266. doi: 10.1007/978-1-4020-9110-0_9.
21. Pozidi-Metaxa E, Athanassiou CG (2013) Comparison of spinosad with three traditional grain protectants against Prostephanus truncatus (Horn) and Ephestia kuehniella (Zeller) at different temperatures. Journal Pest Science 86: 203-210. doi: 10.1007/s10340-012-0445-y.
22. R Development Core Team (2024) R (v4.4.1): A language and environment for statistical computing. The R foundation for statistical computing. Vienna, Austria. https://www.r-project.org.
23. Rosenbaum B, Rall BC (2018) Fitting functional responses: Direct parameter estimation by simulating differential equations. Methods in Ecology and Evolution 9: 2076-2090. doi: 10.1111/2041-210X.13039.
24. Smith SM (1996) Biological control with Trichogramma : Advances, successes, and potential of their use. Annual Review of Entomology 41: 375-406. doi: 10.1146/annurev.en.41.010196.002111.
25. Tonğa A, Bayram A (2021) Natural parasitism of maize stemborers, Sesamia spp. (Lepidoptera: Noctuidae) eggs by Trichogramma evanescens (Hymenoptera: Trichogrammatidae) in Southeastern Turkey. International Journal of Agriculture Environment and Food Sciences 5: 197-202. doi: 10.31015/jaefs.2021.2.9.
26. Tonğa A (2024) The link between functional response and longevity of Trichogramma evanescens strains indigenous to Türkiye: A comparative assessment of parameters. Journal of Applied Entomology 148: 611-623. doi: 10.1111/jen.13252.
27. Tonğa A, Erkek M (2024) Preimaginal treatment of Trichogramma evanescens and T. pintoi with two novel insecticides, afidopyropen and broflanilide: the lethal, sublethal and transgenerational effects. Journal of Pest Science. doi: 10.1007/s10340-024-01836-4.
28. Tonğa A, Erkek M, Ali J, Fathipour Y, Özder N (2024) A comparative approach for life history and functional response demonstrates similar survival strategies for Trichogramma evanescens and T. pintoi. Pest Management Science. doi: 10.1002/ps.8278.
29. Torres JB, de Freitas Bueno A (2018) Conservation biological control using selective insecticides – A valuable tool for IPM. Biological Control 126: 53-64. doi: 10.1016/j.biocontrol.2018.07.012.
30. Ulrichs C, Mewis I (2004) Evaluation of the efficacy of Trichogramma evanescens Westwood (Hym., Trichogrammatidae) inundative releases for the control of Maruca vitrata F. (Lep., Pyralidae). Journal of Applied Entomology 128: 426-431. doi: 10.1111/j.1439-0418.2004.00867.x.
31. Umetsu N, Shirai Y (2020) Development of novel pesticides in the 21st century. Journal of Pesticide Science 45: 54-74. doi: 10.1584/JPESTICS.D20-201.
32. Venables WN, Ripley BD (2002) Modern applied statistics with S, Statistics and Computing. Springer New York, New York, NY. doi: 10.1007/978-0-387-21706-2.
33. Zhang L, Lyu H, Shi D, Li X, Ma K (2022) Effects of low doses of acetamiprid and afidopyropen on the parasitic function of Lysiphlebia japonica (Ashmead). Chinese Journal of Pesticide Science 24: 1417-1424. doi: 10.16801/J.ISSN.1008-7303.2022.0058.
34. Zhang L, Lv H, Li X, Wan H, He S, Li J, Ma K (2023) Sublethal effects of acetamiprid and afidopyropen on Harmonia axyridis: insights from transcriptomics analysis. Ecotoxicology and Environmental Safety 262: 115203. doi: 10.1016/j.ecoenv.2023.115203.