Sublethal effect of the insecticides Flonicamid and Imidacloprid on the functional response of the parasitoid wasp, Diaeretiella rapae to the cabbage aphid, Brevicoryne brassicae

Document Type : Research Paper

Authors

1 Assistant Professor, Plant Protection Research Department, West Azerbaijan Agricultural and Natural Resources Research and Education Center, AREEO, Urmia, Iran.

2 Assistant professor, Plant Protection Research Department, East Azerbaijan Agricultural and Natural Resources Research and Education Centre, AREEO, Tabriz, Iran.

3 Professor, Plant Protection Research Department, East Azerbaijan Agricultural and Natural Resources Research and Education Centre, AREEO, Tabriz, Iran.

4 Researcher, Plant Protection Research Department, West Azerbaijan Agricultural and Natural Resources Research and Education Center, AREEO, Urmia, Iran.

10.22092/bcpp.2026.372146.414

Abstract

The cabbage aphid, Brevicoryne brassicae, is one of the major pests of the Brassicaceae family for which chemical control is one of the most common management methods. However, the use of these compounds requires careful evaluation within integrated pest management (IPM) programs because of its adverse effects on natural enemies. The parasitoid wasp, Diaeretiella rapae is recognized as an important biological control agent of the cabbage aphid in many regions of the world. In this study, the sublethal effect of the insecticides flonicamid and imidacloprid were evaluated on the functional response of the parasitoid wasp, D. rapae to different densities of third-instar cabbage aphid nymphs to assess pesticide compatibility. A colony of D. rapae was established using mummified aphids collected from cabbage fields in Urmia County and maintained in small ventilated containers (20 mL) under controlled laboratory conditions. All rearing and experiments were conducted at 25 ± 1 °C, 60 ± 5% relative humidity, and a photoperiod of 16:8 h (L:D). Sublethal concentrations of the insecticides were determined using a direct spray method in bioassays (LC₂₅: flonicamid = 0.997 ppm and imidacloprid = 5.612 ppm). In the functional response experiment, different densities of aphid nymphs were exposed to a single female (≤24 h) wasp for 24 hours, and the nymphs were then maintained until mummification to determine the parasitism rate. The results showed that the functional response of D. rapae was type II in the control and flonicamid treatment, and type III in the imidacloprid treatment. The parameters of searching efficiency (a) and handling time (Th) were affected by insecticide treatments; flonicamid (0.456 h-1) had no significant effect on searching efficiency, whereas imidacloprid (0.00375 h-1) significantly reduced it. In addition, handling time increased significantly in both treatments. The maximum attack rate in the flonicamid and imidacloprid treatments for D. rapae was 16.24 and 9.44 aphid nymphs, respectively. Therefore, flonicamid showed greater compatibility with D. rapae compared with imidacloprid and can be used in integrated management programs for the cabbage aphid. However, further studies are necessary on the effects of these insecticides on life table parameters and other behavioral characteristics of the parasitoid under laboratory and field conditions.

Keywords

Main Subjects


Abd El-Kareim, A.I., Ghanim, N.M., El-Gazar, E.E., & Rashed, A.A. 2024. Functional response of the parasitoid Diaeretiella rapae (McIntosh) to different densities of Myzus persicae (Sulzer) under laboratory conditions. Journal of Plant Protection and Pathology, 15(6): 243–248. DOI:https://doi.org/10.21608/jppp.2024.330299.1273
Agathokleous, E., Blande, J.D., Masui, N., Calabrese, E.J., Zhang, J., Sicard, P., Guedes, R.N.C. & Benelli, G. 2023. Sublethal chemical stimulation of arthropod parasitoids and parasites of agricultural and environmental importance. Environmental Research, 237(1): 116876. DOI: https://doi.org/10.1016/j.envres.2023.116876
Akhter, S., Naik, V.K., Naladi, B.J., Rathore, A., Yadav, P. & Lal, D. 2024. The ecological impact of pesticides on non‑target organisms in agricultural ecosystems. Advances in Bioresearch, 15(4): 322–334. DOI:https://doi.org/10.15515/abr.0976‑4585.15.4.322334
Ali, J., Xiao, F., Alam, A., Li, L.J., Ji, Y., Chao, W.H., Weibo, Q., Xie, A., Zengyi, B., Abdel Hafez, M.M., Ghramh, H.A., Khan, K.A., Tonğa, A. & Chen, R. 2024. Prohydrojasmon treatment of Brassica juncea alters the performance and behavioural responses of the cabbage aphid, Brevicoryne brassicae. Entomologia Experimentalis et Applicata, 172(11): 1014–1023. DOI:https://doi.org/10.1111/eea.13506
Amini Jam, N. 2022. Sublethal effects of acetamiprid, pymetrozine and flonicamid on the functional response of Aphidius matricariae Haliday. Plant Protection (Scientific Journal of Agriculture), 45(1): 97-117. DOI:https://doi.org/10.22055/ppr.2022.17400. (In Persian with English summary)
Amini Jam, N. & Kabiri Dehkordi, S. 2018. Effects of spirotetramat, acetamiprid, pirimicarb and flonicamid on parasitoid wasp, Lysiphlebus fabarum (Marshall) (Hym.: Braconidae) under laboratory conditions. Plant Pest Research, 8(2): 67-81. DOI:10.22124/iprj.2018.2996. (In Persian with English summary)
Amini Jam, N., Kocheyli, F., Mossadegh, M. S., Rasekh, A. & Saber, M. 2012. Effect of imidacloprid and pirimicarb on functional response of Aphidius matricariae Haliday (Hym: Braconidae) under laboratory conditions. Plant Pests Research, 2(3): 51-61. (In Persian with English summary)
Bernal, J.S., Bellows, T.S. & Gonzalez, D. 1994. Functional response of Diaeretiella rapae (McIntosh) (Hymenoptera: Aphidiidae) to Diuraphis noxia (Mordwilko) (Homoptera: Aphididae) hosts. Journal of Applied Entomology, 118(3–4): 300–309. DOI:https://doi.org/10.1111/j.1439-0418.1994.tb00804.x
Bommarco, R., Firle, S.O. & Ekbom, B. 2007. Outbreak suppression by predators depends on spatial distribution of prey. Ecological Modelling, 201(2): 163–170. DOI:https://doi.org/10.1016/j.ecolmodel.2006.09.012
Chong, J.-H. & Oetting, R.D. 2006. Functional response and progeny production of the Madeira mealybug parasitoid, Anagyrus sp. nov. nr. sinope: The effects of host and parasitoid densities. Biological Control, 39(3): 320–328. DOI:https://doi.org/10.1016/j.biocontrol.2006.08.013
De Jiu, G. & Waage, J.K. 1990. The effect of insecticides on the distribution of foracing parasitoids, Diaeretiella rapae (Hym.: Braconidae) on plants. Entomophaga, 35(1): 49–56. DOI:https://doi.org/10.1007/BF02374300
Desneux, N., Decourtye, A. & Delpuech, J.-M. 2007. The sublethal effects of pesticides on beneficial arthropods. Annual Review of Entomology, 52: 81–106. DOI:https://doi.org/10.1146/annurev.ento.52.110405.091440
El-Shazly, M., El-Shafie, F. & Mohamed, M. 2021. Impact of the parasitoid, Diaeretiella rapae (McIntosh), on crucifer’s aphid in Egypt and Iraq. Egyptian Academic Journal of Biological Sciences, F. Toxicology & Pest Control, 13(2): 289–299. DOI:https://doi.org/10.21608/eajbsf.2021.243112
Fathipour, Y., Hosseini Gharalari, A. & Talebi, A.A. 2004. Some behavioral characteristics of Diaeretiella rapae (Hym.: Aphidiidae), parasitoid of Brevicoryne brassicae (Hom.: Aphididae). Iranian Journal of Agricultural Sciences, 35(2): 395–401. (In Persian with English summary)
Fathipour, Y., Hosseini, A., Talebi, A. & Moharramipour, S. 2006. Functional response and mutual interference of Diaeretiella rapae (Hymenoptera: Aphidiidae) on Brevicoryne brassicae (Homoptera: Aphididae). Entomologica Fennica, 17(2): 90–97. DOI:https://doi.org/10.33338/ef.84293
Fathipour, Y., Kamali, K., Khalghani, J. & Abdollahi, G. 2001. Functional response of Trissolcus grandis (Hym., Scelionidae) to different egg densities of Eurygaster integriceps (Het., Scutelleridae) and effects of wheat genotypes on it. Applied Entomology and Phytopathology, 68: 123–136.
Fernández‑Arhex, V. & Corley, J.C. 2003. The functional response of parasitoids and its implications for biological control. Biocontrol Science and Technology, 13(4): 403–413. DOI:https://doi.org/10.1080/0958315031000104523
Greenop, A., Woodcock, B.A., Wilby, A., Cook, S.M. & Pywell, R.F. 2018. Functional diversity positively affects prey suppression by invertebrate predators: A meta‑analysis. Ecology, 99(8): 1771-1782. DOI:https://doi.org/10.1002/ecy.2378
Guo, K., Yang, P., Chen, J., Lu, H. & Cui, F. 2017. Transcriptomic responses of three aphid species to chemical insecticide stress. Science China Life Sciences, 60(8): 931–934. DOI:https://doi.org/10.1007/s11427‑017‑9104‑5
Hassell, M.P. 2000. The Spatial and Temporal Dynamics of Host–Parasitoid Interactions. Oxford, UK: Oxford University Press. DOI:https://doi.org/10.1093/oso/9780198540892.001.0001
Holling, C.S. 1959. Some characteristics of simple types of predation and parasitism. The Canadian Entomologist, 91(7): 385–398. DOI:https://doi.org/10.4039/Ent91385-7
Islam, Y., Shah, F.M., Rubing, X., Razaq, M., Yabo, M., Li, X. & Zhou, X. 2021. Functional response of Harmonia axyridis preying on Acyrthosiphon pisum nymphs: The effect of temperature. Scientific Reports, 11: 13565. DOI:https://doi.org/10.1038/s41598‑021‑92954‑x
Juliano, S.A. 2001. Non-linear curve fitting: predation and functional response curves. In S.M. Scheiner & J. Gurevitch (Eds), Design and analysis of ecological experiments (pp. 178-196). Oxford University Press: New York. DOI:https://doi.org/10.1093/oso/9780195131871.003.0010
Kaleem Ullah, R.M., Gao, F., Sikandar, A. & Wu, H. 2023. Insights into the effects of insecticides on aphids (Hemiptera: Aphididae): Resistance mechanisms and molecular basis. International Journal of Molecular Sciences, 24(7): 6750. DOI:https://doi.org/10.3390/ijms24076750
Khakasa, S.W.R., Mohamed, S.A., Lagat, Z.O. Khamis, F.M. & Tanga, C.M. 2016. Host stage preference and performance of the aphid parasitoid Diaeretiella rapae (Hymenoptera: Braconidae) on Brevicoryne brassicae and Lipaphis pseudobrassicae (Hemiptera: Aphididae). International Journal of Tropical Insect Science, 36: 10–21. DOI:https://doi.org/10.1017/S1742758415000260
Knapp, R.A., Doyle, E., Hoffmann, A.A. & Umnia, P.A. 2025. Sub-lethal and population –level impacts of afidopyropen and flonicamid on Harmonia conformis (Coleoptera: Coccinellidae). Ecotoxicology and Environmental Safety, 303: 118958. DOI:https://doi.org/10.1016/j.ecoenv.2025.118958
Kolac, J., Schneider, M.I. & Rimoldi, F. 2024. Short- and long-term effects of commercial formulations of imidacloprid, spirotetramat, and mixtures of these active ingredients on pupae of Diaeretiella rapae (Hymenoptera: Braconidae) and its progeny. Pest Management Science, 80(9): 4594-4603. DOI:https://doi.org/10.1002/ps.8178
Lester, P.J. & Harmsen, R. 2002. Functional and numerical responses do not always indicate the most effective predator for biological control: An analysis of two predators in a two‑prey system. Journal of Applied Ecology, 39(3): 455–468. DOI:https://doi.org/10.1046/j.1365-2664.2002.00733.x
Mahmoodi, L., Mehrkhou, F., Guz, N., Forouzan, M. & Atlihan, R. 2020. Sublethal effects of three insecticides on fitness parameters and population projection of Brevicoryne brassicae (Hemiptera: Aphididae). Journal of Economic Entomology, 113(6): 2713–2722. DOI:https://doi.org/10.1093/jee/toaa193
Marandi, R., Safavi, S.A., Forouzan, M. & Jarrahi, A. 2025. Fertility life table parameters of the cabbage aphid, Brevicoryne brassicae affected by sublethal concentration of BotanAphid aphidicide on two cabbage varieties. Plant Protection (Scientific Journal of Agriculture), 47(4): 23-43. DOI:https://doi.org/10.22055/ppr.2024.48256.1772. (In Persian with English summary)
Messina, F.J. & Hanks, J.B. 1998. Host plant alters the shape of functional response of an aphid predator (Coleoptera: Coccinellidae). Environmental Entomology, 27(5): 1196–1202. DOI:https://doi.org/10.1093/ee/27.5.1196
Moayeri, H.R.S., Madadi, H., Pouraskari, H. & Enkegaard, A. 2013. Temperature-dependent functional response of Diaeretiella rapae (Hymenoptera: Aphidiidae) to the cabbage aphid, Brevicoryne brassicae (Hemiptera: Aphididae). European Journal of Entomology, 110(1): 109–113. DOI:https://doi.org/10.14411/eje.2013.015
Nisar, S. & Rizvi, P.Q. 2021. Host fitness of different aphid species for Diaeretiella rapae (M’Intosh): a life table approach. International Journal of Tropical Insect Science, 41: 787–799. DOI:https://doi.org/10.1007/s42690-020-00269-7
Núñez-Campero, S.R., Suárez, L.d.C., Mello García, F.R., Cancino, J., Montoya, P. & Ovruski, S.M. 2025. Insights into the functional responses of four Neotropical-native parasitoids to enhance their role as biocontrol agents against Anastrepha fraterculus pest populations. Insects, 16(9): 919. DOI:https://doi.org/10.3390/insects16090919
Pandey, K.P., Singh, R. & Tripathi, C.P.M. 1984. Functional response of Diaeretiella rapae (M’Intosh) (Hym., Aphidiidae), a parasitoid of the mustard aphid Lipaphis erysimi Kalt. (Hom., Aphididae). Journal of Applied Entomology, 98(4): 321–327. DOI:https://doi.org/10.1111/j.1439-0418.1984.tb02718.x
Papanikolaou, N.E., Kypraios, T., Moffat, H., Fantinou, A., Perdikis, D.P. & Drovandi, C. 2021. Predators’ functional response: Statistical inference, experimental design, and biological interpretation of the handling time. Frontiers in Ecology and Evolution, 9: 740848. DOI:https://doi.org/10.3389/fevo.2021.740848
Pervez, A. & Omkar. (2005). Functional responses of coccinellid predators: An illustration of a logistic approach. Journal of Insect Science, 5(1): 5. DOI:https://doi.org/10.1093/jis/5.1.5
Radrigán-Navarro, C. & Fuentes-Contreras, E. 2024. Sublethal effects of insecticides on the parasitism of Acerophagus flavidulus, a parasitoid of Pseudococcus viburni. Sustainability, 16(4): 1478. DOI:https://doi.org/10.3390/su16041478
Rezaei, N., Kocheyli, F., Mossadegh, M.S., Talebi Jahromi, KH. & Kavousi, A. 2014. Effect of sublethal doses of thiamethoxam and pirimicarb on functional response of Diaeretiella rapae (Hymenoptera: Braconidae), parasitoid of Lipaphis erysimi (Hemiptera: Aphididae), Journal of Crop Protection, 3(4): 467-477. DOI:https://doi.org/ 10.48311/jcp.2014.1156
Rogers, D. (1972). Random search and insect population models. Journal of Animal Ecology, 41: 369-383. DOI:https://doi.org/10.2307/3474
Schmidt‑Jeffris, R.A., Beers, E.H. & Sater, C. 2021. Meta‑analysis and review of pesticide non‑target effects on phytoseiids, key biological control agents. Pest Management Science, 77(11): 4848–4862. DOI:https://doi.org/10.1002/ps.6531
Siddiqui, J.A., Fan, R., Naz, H., Bamisile, B.S., Hafeez, M., Ghani, M.I., Wei, Y., Xu, Y. & Chen, X. (2023). Insights into insecticide‑resistance mechanisms in invasive species: Challenges and control strategies. Frontiers in Physiology, 13: 1112278. DOI:https://doi.org/10.3389/fphys.2022.1112278
Slavíková, L., Fryč, D. & Kundu, J.K. 2024. Analysis of twenty years of suction trap data on the flight activity of Myzus persicae and Brevicoryne brassicae, two main vectors of oilseed rape infection viruses. Agronomy, 14(9): 1931. DOI:https://doi.org/10.3390/agronomy14091931
Soni, S. & Kumar, S. 2021a. Biological control potential of an aphid parasitoid, Diaeretiella rapae (McIntosh) (Hymenoptera: Braconidae) against Brevicoryne brassicae (Linnaeus) (Hemiptera: Aphididae), a pest of oilseed brassicas in India. International Journal of Tropical Insect Science, 41(4): 2361–2372. DOI:https://doi.org/10.1007/s42690‑020‑00408‑0
Soni, S. & Kumar, S. 2021b. Efficacy of the parasitoid, Diaeretiella rapae (McIntosh) (Hymenoptera: Braconidae) against Myzus persicae (Sulzer) (Hemiptera: Aphididae) infesting rapeseed-mustard. Journal of Asia‑Pacific Entomology, 24(3): 912–917. DOI:https://doi.org/10.1016/j.aspen.2021.07.019
Stanley, J. & Preetha, G. 2024. Investigating the effect of chlorpyriphos and spirotetramat insecticides on the functional response of Aenasius bambawalei. Entomology and Applied Science Letters, 11(2): 40–47. DOI:https://doi.org/10.51847/uVDdv6yrPt
Talebi, A.A., Kazemi, M., Rezaei, M., Mirhosseini, M.A. & Moharramipour, S. 2021. Host stage preference and temperature‑dependent functional response of Diaeretiella rapae (Hymenoptera: Braconidae) on Schizaphis graminum (Hemiptera: Aphididae). International Journal of Tropical Insect Science, 42(1): 415–424. DOI:https://doi.org/10.1007/s42690‑021‑00558‑9
Tazerouni, Z., Talebi, A.A. & Rakhshani, E. 2011. The foraging behavior of Diaeretiella rapae (Hymenoptera: Braconidae) on Diuraphis noxia (Hemiptera: Aphididae). Archives of Biological Sciences, 63(1): 225–234. DOI:https://doi.org/10.2298/ABS1101225T
Tazerouni, Z., Talebi, A.A. & Rakhshani, E. 2012. Temperature‑dependent functional response of Diaeretiella rapae (Hymenoptera: Braconidae), a parasitoid of Diuraphis noxia (Hemiptera: Aphididae). Journal of the Entomological Research Society, 14(1): 31–40. DOI:https://entomol.org/journal/index.php/JERS/article/view/343
Teder, T. & Knapp, M. 2019. Sublethal effects enhance detrimental impact of insecticides on non-target organisms: A quantitative synthesis in parasitoids. Chemosphere, 214: 371-378. DOI:https://doi.org/10.1016/j.chemosphere.2018.09.132
Tomasetto, F., Casanovas, P., Brandt, S.N. & Goldson, S.L. 2018. Biological control success of a pasture pest: Has its parasitoid lost its functional mojo? Frontiers in Ecology and Evolution, 6: 215. DOI:https://doi.org/10.3389/fevo.2018.00215
Trexler, J.C., McCulloch, C.E. & Travis, J. 1988. How can the functional response best be determined? Oecologia, 76(2): 206–214. DOI:https://doi.org/10.1007/BF00379954
Trexler, J. C. & Travis, J. 1993. Nontraditional regression analysis. Ecology, 74(6): 1629–1637. DOI:https://doi.org/10.2307/1939921
Theenoor, R., Ghosh, A. & Venkatesan, R. 2024. Harmonising control: Understanding the complex impact of pesticides on parasitoid wasps for enhanced pest management. Current Opinion in Insect Science, 65: 101236. DOI:https://doi.org/10.1016/j.cois.2024.101236
Wu, J., Li, G., Lin, Z., Zhang, Y., Yu, W., Hu, R., Zhan, S. & Chen, Y. 2025. A chromosome-level genome assembly of the cabbage aphid Brevicoryne brassicae. Scientific Data, 12: 167. DOI:https://doi.org/10.1038/s41597-025-04501-2
Yu, X.-L., Tang, R., Xia, P.-L., Wang, B., Feng, Y. & Liu, T.-X. 2020. Effects of prey distribution and heterospecific interactions on the functional response of Harmonia axyridis and Aphidius gifuensis to Myzus persicae. Insects, 11(6): 325. DOI:https://doi.org/10.3390/insects11060325
Zhang, W. & Swinton, S.M. 2009. Incorporating natural enemies in an economic threshold for dynamically optimal pest management. Ecological Modelling, 220(9-10): 1315–1324. DOI:https://doi.org/10.1016/j.ecolmodel.2009.01.027
Zhou, W., Arcot, Y., Medina, R.F., Bernal, J., Cisneros-Zevallos, L., & Akbulut, M.E.S. 2024. Integrated Pest Management: An update on the sustainability approach to crop protection. ACS Omega, 9(40): 41130–41147. DOI:https://doi.org/10.1021/acsomega.4c06628