Delayed reproductive behavioral responses in Drosophila melanogaster (Diptères: Drosophilidae) fFollowing exposure to aqueous extract of Peganum harmala and the insecticide Spinosad

Document Type : Paper, English

Authors

1 Ecology Laboratory of Marine and Coastal Environments (EMMAL), Department of Biology, Faculty of Sciences, Badji Mokhtar – Annaba University BP 12, P.O. Box 23000, Annaba, Algeria

2 Genetics, Biotechnology and Bioresources valorization Laboratory Department of Nature and Life Sciences, Faculty of Exact Sciences and Sciences of Nature and Life, Mohamed Kheider University, Biskra, Algeria

3 Ecosystem Diversity and Dynamics of Agricultural Production Systems in Arid Zones Laboratory Department of Agriculture Sciences, Faculty of Exact Sciences and Sciences of Nature and Life, Mohamed Kheider University, Biskra, Algeria

10.22034/jesi.46.2.2

Abstract

This study aims to evaluate the delayed effects of two treatments spinosad (a commercially available insecticide) and a natural bioinsecticide (aqueous extract of Peganum harmala) on the sexual behavior and oviposition of vinegar flies (Drosophila melanogaster). Sublethal concentrations (86 mg/ml P. harmala, 0.020 mg/ml Spinosad) of each product were administered via ingestion to second-instar (L2) larvae of D. melanogaster. The results indicated that exposure to Spinosad significantly reduced sexual activity in D. melanogaster, as evidenced by prolonged mating latency and a lower copulation rate. Moreover, its repellent properties alter female oviposition site preference and a marked decrease in the number of eggs laid. In contrast, the natural bioinsecticide (aqueous extract of P. harmala) exerted a milder effect: it reduced the frequency of courtship behaviors; it prevented mating in most individuals. Its moderate repellent effect also influenced oviposition site selection, leading to reduction in egg deposition.

Graphical Abstract

Delayed reproductive behavioral responses in Drosophila melanogaster (Diptères: Drosophilidae) fFollowing exposure to aqueous extract of Peganum harmala and the insecticide Spinosad

Keywords

Main Subjects

Article Title [Persian]

تاثیر عصاره آبی گیاه اسپند (Peganum harmala) و حشره‌کش اسپینوساد در بروز پاسخ‌های رفتاری تولید مثلی با تأخیر در Drosophila melanogaster (Dip., Drosophilidae)

Authors [Persian]

  • خمسه کریمچه 1
  • ایسمانه لبوز 2
  • رچا بناچن 1
  • رشید کرچید 1
  • اینس کیهل 1
  • منیر بومایزی 1
  • یاسمین عجمی 1
  • ایوب حاجب 3
  • محمد لید اوکید 1
1 آزمایشگاه بوم‌شناسی محیط‌های دریایی و ساحلی، گروه زیست‌شناسی، دانشکده علوم، دانشگاه باجی مختار عنابه، عنابه، الجزایر
2 آزمایشگاه ارزش‌گذاری ژنتیک، بیوتکنولوژی و منابع زیستی، گروه علوم طبیعی و زیستی، دانشکده علوم دقیق، علوم طبیعی و زیستی، دانشگاه محمد خیدر، بسکره، الجزایر
3 آزمایشگاه تنوع اکوسیستم و پویایی سیستم‌های تولید کشاورزی در مناطق خشک، گروه علوم کشاورزی، دانشکده علوم دقیق ، علوم طبیعی و زیستی، دانشگاه محمد خیدر، بسکره، الجزایر
Abstract [Persian]

این مطالعه با هدف ارزیابی اثرات تأخیری دو تیمار اسپینوساد (حشره‌کش تجاری رایج) و یک حشره‌کش زیستی طبیعی (عصاره آبی Peganum harmala) بر رفتار جنسی و تخم‌گذاری مگس سرکه (Drosophila melanogaster) انجام شد. غلظت‌های زیرکشنده (86 میلی‌گرم در میلی‌لیتر اسپینوساد، 0.020 میلی‌گرم در میلی‌لیتر اسپینوساد) از هر ترکیب از طریق بلع به لاروهای سن دوم D. melanogasterخورانده شد. نتایج نشان داد که قرار گرفتن در معرض اسپینوساد، فعالیت جنسی مگس سرکه D. melanogaster را بطور قابل توجهی کاهش داده و منجر به تأخیر طولانی مدت جفت‌گیری شده و میزان جفت‌گیری نیز کاش محسوسی داشت. علاوه بر این، خواص دفع‌کنندگی اسپینوزاد، روی ترجیح محل تخم‌گذاری ماده‌ها اثر گذاشته و منجر به کاهش قابل توجه تعداد تخم‌های گذاشته شده می‌گردد. در مقابل، حشره‌کش زیستی طبیعی (عصاره آبی اسپند) اثر ملایم‌تری داشت. به نحوی که فراوانی رفتارهای جفت‌خوانی را کاهش داد و در بیشتر افراد از جفت‌گیری جلوگیری کرد. اثر دورکنندگی متوسط این ترکیب نیز بر انتخاب محل تخم‌گذاری تأثیر گذاشت و منجر به کاهش تخم‌گذاری شد.

Keywords [Persian]

  • آفت‌کش‌های طبیعی
  • غلظت زیرکشنده
  • رفتار جفت‌گیری
  • تخم‌گذاری
  • آفت‌کش گیاهی

© 2026 by Author(s), Published by the Entomological Society of Iran

This Work is Licensed under Creative Commons Attribution-Non-Commercial 4.0 International Public License.

References

Abbasipour, H., Mahmoudvand, M., Rastegar, F. &Basij, M. (2010) Insecticidal activity of Peganum harmala seed extract against the diamondback moth, Plutella xylostella. Bulletin of Insectology, 63(2), 259–263.
Ahmed, N., Alam, M., Saeed, M., Ullah, H., Iqbal, T., Al-Mutairi, K. A., Shahjeer, k., Ullah, R., Ahmed,S., Ahmed, N. A. H., Khater, H. F.& Salman, M. (2021) Botanical insecticides are a non-toxic alternative to conventional pesticides in the control of insects and pests. In Global Decline of Insects. IntechOpen. https://doi.org/10.5772/intechopen.100416
Agrawal,S., Safarik,S. & Dickinson,. M. (2014) The relative roles of vision and chemosensation in mate recognition of Drosophila melanogaster. Journal of Experimental Biology. 217.15: 2796–2805. https://doi.org/10.1242/jeb.105817
Ai, T., Phien, H. & Men, T. (2021) Phytochemical constituents and toxicity of the ethanol extract of Ricinus communis (L.) in Drosophila melanogaster. Asian Journal of Biology, 13, 12–21.DOI: 10.9734/AJOB/2021/v13i430192
Amrani, S., Habbachi, S., Benhissen, S., Rebbas, K. &Habbachi, W. (2022) Evaluation of insecticidal effects of Ruta chalepensis ethanolic extract on mortality, sexual behaviour, and oviposition of Drosophila melanogaster (Diptera: Drosophilidae). Asia Life SciencesEvaluation, 12(11). https://www.researchgate.net/publication/365126582
Bartling, M. T., Brandt, A., Hollert, H. & Vilcinskas, A. (2024) Current insights into sublethal effects of pesticides on insects. International Journal of Molecular Sciences, 25 (11), 6007. https://doi.org/10.3390/ijms25116007
Begum, J. & Islam, W. (2022) Toxic and repellent potentials of spinosad against Cryptolestes pusillus (Schon.) (Coleoptera: Cucujidae). International Journal of Biological and Pharmaceutical Sciences Archive.  https://doi.org/10.53771/ijbpsa.202.3.2.0042
Benhissen, S.,Habbachi, W., Hedjouli, Z., Asloum, A.&Bounadji, S. (2023) Effects of Spinosad and Bacillus thuringiensis kurstaki on Culex pipiens Linnaeus, 1758 (Diptera: Culicidae): Adults’ fertility, fecundity and cuticular hydrocarbons.Acta Zoologica Bulgarica, 75(2).265-272.
Boulahbel, B.,Aribi, N., Kilani-Morakchi, S. & Soltani, N. (2015) Insecticidal activity of azadirachtin on Drosophila melanogaster and recovery of normal status by exogenous 20-hydroxyecdysone.African Entomology, 23(1), 224–233. https://hdl.handle.net/10520/EJC167507
Chowańskia, S., Chudzińskac, E., Lelariod, F., Ventrellad, E., Marciniaka, P., Miądowicz-Kobielskac, M., Spochacza, M., Szymczaka, M., Scranoe, S. L., Bufod, S. A.& Adamskia, Z. (2018) Insecticidal properties of Solanum nigrum and Armoracia rusticana extracts on reproduction and development of Drosophila melanogaster. Ecotoxicology and Environmental Safety, 162, 454-463. https://doi.org/10.3390/toxins10120504
Clemens, J., Coen, P., Roemschied, F. A., Pereira, T. D., Mazumder, D., Aldarondo, D. E., Pacheco, D. A. &Murthy, M. (2018) Discovery of new song mode in Drosophila hidden structure in the sensory and neural drivers of behavior. Current Biology, 28(15), 2400–2412.doi: 10.1016/j.cub.2018.06.011
Coen, P., Xie, M., Clemens, J. & Murthy, M. (2016)Sensorimotor transformations underlying variability in song intensity during Drosophila courtship. Neuron, 89(3), 629–644.https://doi.org/10.1016/j.neuron.2015.12.035
CSAN Niger. (2017). Classification des pesticides et des acaricides selon le mode d’action. IPMnote, 1. http://www.exemple.org/spino.pdf
David, J. (1963) Influence of female fertilization on the number and size of eggs laid: A study in Drosophila melanogaster Meigen. Journal of Insect Physiology, 9(1), 13–24. http://dx.doi.org/10.1016/0531-5565(75)90011-X
El-Bah, D., Habbachi, W., Ouakid, M. L. &Tahraoui, A. (2016) Sublethal effects of Peganum harmala (Zygophyllaceae) on sexual behavior and oviposition in fruit fly Drosophila melanogaster (Diptera: Drosophilidae). Journal of Entomology and Zoology Studies, 4(6), 638–642.
Gorter, J. A. &Billeter, J. C. (2017) A method to test the effect of environmental cues on mating behavior in Drosophila melanogaster. Journal of Visualized Experiments: JoVE, (125), 55690. https://dx.doi.org/10.3791/55690
Greenspan, R. J. (1995) Understanding the genetic construction of behavior. Scientific American, 272(4), 72–78.
Greenspan, R. J. & Ferveur, J. F. (2000)Courtship in Drosophila. Annual Review of Genetics, 34(1), 205-232.https://doi.org/10.1146/annurev.genet.34.1.205
Grillet, M., Dartevelle, L. &Ferveur, J. F. (2005)A Drosophila male pheromone affects female sexual receptivity. Proceedings of the Royal Society B: Biological Sciences, 273(1584), 315–323. https://doi.org/10.1098/rspb.2005.3332
Hartmann, T. (1991) Alkaloids In herbivores; their interaction with secondary plant metabolites. The Chemical Participants, 1, 2. https://doi.org/10.1111/j.1570-7458.1996.tb00914.x
Hegde, S. N. & Krishnamurthy, N. B. (1979) Studies on mating behaviour in the Drosophila bipectinata complex. Australian Journal of Zoology, 27(3), 421-431. https://doi.org/10.1071/ZO9790421
Kartal, M., Altun, M. L. &Kurucu, S. (2003) HPLC method for the analysis of harmol, harmalol, harmine and harmaline in the seeds of Peganum harmala L. Journal of Pharmaceutical and Biomedical Analysis, 31(2), 263–269. https://doi.org/10.1016/S0731-7085(02)00568-X
Kihel, I., Merabeti, B., Adjami, Y., Boumaza, M., Gouri, M., Bouzdoğan, H. &Ouakid, M. L. (2022) Toxicity and sexual behavior in fruit fly Drosophila melanogaster (Diptera: Drosophilidae) treated with the fruit extract of Citrullus colocynthis. Current Topics in Toxicology, 18(14), 113–121.
Kissoum, N., Bensafi-Gheraibia, H., Hamida, Z. C. & Soltani, N. (2020) Evaluation of the pesticide Oberon on a model organism Drosophila melanogaster via topical toxicity test on biochemical and reproductive parameters. Comparative Biochemistry and Physiology Part C: Toxicology and Pharmacology, 228,108666.       https://doi.org/10.1016/j.cbpc.2019.108666
Kushalan, S., D’Souza, L. C., Aloysius, K., Sharma, A. & Hegde, S. (2022) Toxicity assessment of Curculigo orchioides leaf extract using Drosophila melanogaster: a preliminary study. International Journal of Environmental Research and Public Health, 19(22), 15218.https: //doi.org /10.3390 /ijerph 192215218
Liimatainen, J. O. &Hoikkala, A. (1998) Interactions of the males and females of three sympatric Drosophila virilis-group species, D. montana, D. littoralis, and D. lummei, (Diptera: Drosophilidae) in intra-and interspecific courtships in the wild and in the laboratory. Journal of Insect Behavior, 11(3), 399–417. https://doi.org/10.1023/A:1020906815133
Liu, T., Dartevelle, L., Yuan, C., Wei, H., Wang, Y., Ferveur, J. F. & Guo, A. (2008) Increased dopamine level enhances male–male courtship in Drosophila. Journal of Neuroscience, 28(21), 5539–5546. https://doi.org/10.1523/JNEUROSCI.5290-07.2008
Mahmoudian, M., Salehian, P. &Jalilpour, H. (2002) Toxicity of Peganum harmala: review and a case report. Iranian Journal of Pharmacology and Therapeutic (ijpt), 1(1), 1–4. sid. https://sid.ir/paper/297031/en
Mandi, M., Khatun, S., Rajak, P., Mazumdar, A. & Roy, S. (2020) Potential risk of organophosphate exposure in male reproductive system of a non-target insect model Drosophila melanogaster.  Environmental Toxicology and Pharmacology, 74, 103308. https://doi.org/10.1016/j.etap.2019.103308
McKinney, R. M., Vernier, C. & Ben-Shahar, Y. (2015) The neural basis for insect pheromonal communication. Current opinion in Insect Science, 12, 86–92. https://doi.org/10.1016/j.cois.2015.09.010
Mertz, F. P. & Yao, R. C. (1990) Saccharopolyspora spinosa sp. nov. isolated from soil collected in a sugar mill rum still. International Journal of Systematic and Evolutionary Microbiology, 40(1), 34–39. https://doi.org/10.1099/00207713-40-1-34
Michaelakis, A., Papachristos, D. P., Rumbos, C. I. & Athanassiou, C. G. (2018) Effect of the combined application of microencapsulated synthetic oviposition pheromone (MSP) with different larvicidal agents on the oviposition of Culex pipiens biotype molestus. Pest Management Science, 74(2), 392–397. https://doi.org/10.1002/ps.4719
Nauen, R., Slater, R., Sparks, T. C., Elbert, A. & Mccaffery, A. (2019) IRAC: insecticide resistance and mode of action classification of insecticides. Modern Crop Protection Compounds, 3,995–1012. https://doi.org/10.1002/9783527699261.ch28
Pavlova, A. K., Dahlmann, M., Hauck, M. &Reineke, A. (2017) Laboratory bioassays with three different substrates to test the efficacy of insecticides against various stages of Drosophila suzukii (Diptera: Drosophilidae). Journal of Insect Science, 17(1), 8. https://doi.org/10.1093/jisesa/iew100
Pineda, S., Schneider, M. I., Smagghe, G., Martínez-Castillo, A. M., Del Estal, P., Viñuela, E., Mora, J. F. V. & Budia, F. (2007) Lethal and sublethal effects of methoxyfenozide and spinosad on Spodoptera littoralis (Lepidoptera: Noctuidae). Journal of Economic Entomology, 100(3), 773–780. https://doi.org/10.1093/jee/100.3.773
Piri, F., Sahragard, A. & Ghadamyari, M. (2014) Sublethal effects of Spinosad on some biochemical and bBiological parameters of Glyphodes pyloalisWalker (Lepidoptera: Pyralidae). Plant Protection Science, 50(3), 135–144.
Quiroz-Carreño, S., Pastene-Navarrete, E., Espinoza-Pinochet, C., Muñoz-Núñez, E., Devotto-Moreno, L., Céspedes-Acuña, C. L. &Alarcón-Enos, J. (2020) Assessment of insecticidal activity of benzylisoquinoline alkaloids from Chilean Rhamnaceae plants against fruit-fly Drosophila melanogaster and the lepidopteran crop pest Cydia pomonella. Molecules, 25(21), 5094. https://doi.org/10.3390/molecules 25215094
Reckhaus, H. D. (2019) Why Every Fly Counts. Springer Cham, Suisse, page 53 – 87. https://doi.org/10.1007/978-3-030-31229-9
Rehman, J. U., Wang, X. G., Johnson, M. W., Daane, K. M., Jilani, G., Khan, M. A. &Zalom, F. G. (2009) Effects of Peganum harmala (Zygophyllaceae) seed extract on the olive fruit fly (Diptera: Tephritidae) and its larval parasitoid Psyttalia concolor (Hymenoptera: Braconidae). Journal of Economic Entomology, 102(6), 2233–2240. https://doi.org/10.1603/029.102.0628
Renou, M., Henninot‐Rodes, E., Delorme, R., Augé, D. & Touton, P. (1997) Oviposition of resistant and susceptible strains of Drosophila melanogaster in the presence of deltamethrin. Entomologia Experimenta et Applicata, 84(2), 173-181. https://doi.org/10.1046/j.1570-7458.1997.00212.x
Saadane, F. Z., Habbachi, W., Habbachi, S., Boublata, N. E. I., Slimani, A. &Tahraoui, A. (2021) Toxic effects of ethanolic extracts of Drimia maritima (Asparagaceae) on mortality, development, sexual behavior, and oviposition behavior of Drosophila melanogaster (Diptera: Drosophilidae). Journal of Animal Behaviour and Biometeorology, 9(1), 2102. https://doi.org/10.31893/jabb.21002
Sethuraman, A., Janzen, F. J., Weisrock, D. W. &Obrycki, J. J. (2020) Insights from population genomics to enhance and sustain biological control of insect pests. Insects, 11(8), 462.  https://doi.org/10.3390/insects11080462
Shaw, B., Hemer, S., Cannon, M. F., Rogai, F. & Fountain, M. T. (2019) Insecticide control of Drosophila suzukii in commercial sweet cherry crops under cladding. Insects, 10(7), 196. https://doi.org/10.3390/insects10070196
Sparks, T. C.&Nauen, R. (2015) IRAC: Mode of action classification and insecticide resistance management. Pesticide Biochemistry and Physiology, 121, 122–128. https://doi.org/10.1016/j.pestbp.2014.11.014
Sparks, T. C., Thompson, G. D., Kirst, H. A., Hertlein, M. B., Larson, L. L., Worden, T. V. & Thibault, S. T. (1998) Biological activity of the spinosyns, new fermentation derived insect control agents, on Tobacco budworm (Lepidoptera: Noctuidae) larvae. Journal of Economic Entomology, 91(6), 1277–1283
Spieth, H. T. & Ringo, J. M. (1983).  Mating behavior and sexual isolation in Drosophila. In Ashburner M., Carson, H. L. &Thompson, J.R., Thompson, J. N. (editorrs.), The genetics and biology of Drosophila. 223 – 284. Academic Press, London.
Vaillant, J. & Derridj, S. (1992) Statistical analysis of insect preference in two-choice experiments.  Journal of Insect Behavior, 5(6), 773–781.  https://doi.org/10.1007/BF01047986
Vayias, B. J., Athanassiou, C. G., Milonas, D. N. &Mavrotas, C. (2010) Persistence and efficacy of spinosad on wheat, maize and barley grains against four major stored product pests. Crop Protection, 29(5), 496–505. https://doi.org/10.1016/j.cropro.2009.12.003
Vosshall, L. B. (2008) Scent of a fly. Neuron, 59(5), 685–689. https://doi.org/10.1016/j.neuron.2008.08.014
Watson, G. B. (2001) Actions of insecticidal spinosyns on γ-aminobutyric acid responses from small-diameter cockroach neurons. Pesticide Biochemistry and Physiology, 71, 20–28. https://doi.org/10.1006/pest.2001.2559
Wink, M. (1988) Plant breeding: Importance of plant secondary metabolites for protection against pathogens and herbivores. Theoretical and Applied Genetics, 75, 225–233.
Yao, S., Yang, Y., Xue, Y., Zhao, W., Liu, X., Du, M., Yin, X., Guan, R., Wei, J.& An, S. (2021) New insights on the effects of spinosad on the development of Helicoverpa armigera. Ecotoxicology and Environmental Safety, 221, 112452. https://doi.org/10.1016/j.ecoenv.2021.112452
Yee, W. L. (2018) Spinosad versus spinetoram effects on kill and oviposition of Rhagoletis indifferens (Diptera: Tephritidae) at differing fly ages and temperatures. Journal of Insect Science, 18(4), 15. https://doi.org/10.1093/jisesa/iey082
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.
Zhang, X., Meng, F., Xu, H., Wei, L., Wang, Y., Huang, X.& Wang, D. (2025) Lethal and sublethal effects of spinosad on the dengue mosquito vector, Aedes albopictus, and the Bancroftian Filariasis mosquito vector, Culex pipiens pallens. Journal of Vector Borne Diseases, 62(1), 39–44.DOI: 10.4103/JVBD. JVBD_58_24
Send comment about this article
CAPTCHA Image
Journal of Entomological Society of Iran
Volume 46, Issue 2
April 2026
Pages 147-162

Files

Share

How to cite

Statistics