Azadirachtine maruz kalan Achroia grisella (Fabricius, 1794) (Lepidoptera: Pyralidae) larvalarında ölüm oranı, gelişim biyolojisi ve hücresel bağışıklık tepkileri

Year 2022, Volume: 46 Issue: 4, 441 - 452, 07.01.2023

Aylin Er

https://doi.org/10.16970/entoted.1123238

Cited By: 1

Abstract

Neem ağaçlarından elde edilen Azadirachtin, direnç sorunu olmayan ve tarımsal zararlıların kontrolü için sentetik pestisitlere güçlü bir alternatif oluşturmaktadır. Küçük mum güvesi Achroia grisella (Fabricius, 1794) (Lepidoptera: Pyralidae)’da ölüm, gelişim biyolojisi ve hücresel bağışıklık göstergeleri üzerindeki azadirachtin kaynaklı etkiler değerlendirilmiştir. Denemeler kontrollü laboratuvar ortamında Balıkesir Üniversitesi’nde gerçekleştirilmiştir. Azadirachtinin topikal uygulamasına bağlı olarak LD50 0.02 mg/ml bulunurken, PD50 (pupa dönemine geçmeden ölümler) 0.05 mg/ml olarak tespit edildi. 0.05 mg/ml ve 0.1 mg/ml'de larva dönemi ve ergin çıkış süresi, önemli ölçüde artarken, pupa dönemindeki uzama sadece 0.1 mg/ml'de önemli bulunmuştur. Ergin çıkış oranları ve ergin yaşam süresi, kullanılan tüm dozlarda azalmıştır. Azadirachtinin topikal uygulaması, uygulamadan 24 ve 48 saat sonra dolaşımdaki hemosit sayılarında ve hemosit yayılma davranışında önemli bir azalmaya neden olurken, plazmatosit ve granülosit sayılarındaki varyasyonlar istatistiksel olarak anlamlı bulunmamıştır. Achroia grisella ile mücadelede azadirachtinin potansiyel etkileri olmakla birlikte, agroekosistemlerde güvenli kullanımının önerilmesi için parazitoitler ve predatörler gibi biyolojik kontrol ajanları üzerindeki etkilerinin belirlenmesi önem arz etmektedir.

Keywords

Achroia grisella, azadirachtin, hemosit sayısı, toksisite

Project Number

Grant Project No: 2018/088

Mortality, developmental biology and cellular immunity in Achroia grisella (Fabricius, 1794) (Lepidoptera: Pyralidae) larvae exposed to azadirachtin

Abstract

Azadirachtin, obtained from neem trees, can be a robust alternative to synthetic pesticides for the control of agricultural pests with no resistance problems. Azadirachtin-induced influences on mortality, life history traits and cellular immunity indicators of the lesser wax moth Achroia grisella (Fabricius, 1794) (Lepidoptera: Pyralidae) were evaluated. The experiments were conducted under controlled laboratory conditions at Balıkesir University. The topical application of azadirachtin gave an LD50 of 0.02 mg/ml whereas the PD50 (deaths without pupation) was 0.05 mg/ml. The prolongation of the larval stage and adult emergence time was significantly increased at 0.05 mg/ml and 0.1 mg/ml while the duration of the pupal stage was only significant at 0.1 mg/ml. Adult emergence ratios and longevity were reduced at all doses. Topical application of azadirachtin caused a marked decrease in the number of circulating hemocyte counts and spreading ability 24 and 48 h after treatment, however, the variations in plasmatocyte and granulocyte counts were not significant. Although azadirachtin has potential effects in the control of A. grisella, its effects on biological control agents such as parasitoids and predators must be determined to recommend its safe use in agroecosystems.

Keywords

Achroia grisella, azadirachtin, hemocyte count, toxicity

Supporting Institution

Balıkesir University, Scientific Research Coordination Unit, Türkiye

Project Number

Grant Project No: 2018/088

References

• Adel, M. M. & F. Sehnal, 2000. Azadirachtin potentiates the action of ecdysteroid agonist RH-2485 in Spodoptera littoralis. Journal of Insect Physiology, 46 (3): 267-274.
• Akthar, Y., M. B. Isman, L. A. Niehaus, C. H. Lee & H. S. Lee, 2012. Anti- feedant and toxic effects of naturally occurring and synthetic quinones to the cabbage looper, Trichoplusia ni. Crop Protection, 31 (1): 8-14.
• Altuntaş, H., F. Uçkan, A. Y. Kiliç & E. Ergin, 2014. Effects of gibberellic acid on hemolymph-free amino acids of Galleria mellonella (Lepidoptera: Pyralidae) and endoparasitoid Pimpla turionellae (Hymenoptera: Ichneumonidae). Annals of the Entomological Society of America, 107 (5): 1000-1009.
• Amaral, K. D., L. C. Gandra, M. A. de Oliveira, D. J. de Souza & T. M. C. Della Lucia, 2019. Effect of azadirachtin on mortality and immune response of leaf-cutting ants. Ecotoxicology, 28 (10): 1190-1197.
• Amaral, K. D., L. C. Martinez, M. A. P. Lima, J. E. Serrão & T. M. C. Della Lucia, 2018. Azadirachtin impairs egg production in Atta sexdens leaf-cutting queens. Environmental Pollution, 243 (Part B): 809-814.
• Azambuja, P., E. S. Garcia, N. A. Ratcliffe & J. D. Warthen, 1991. Immune- depression in Rhodnius prolixus induced by the growth inhibitor, azadirachtin. Journal of Insect Physiology, 37 (10): 771-777.
• Barbosa, W. F., L. De Meyer, R. N. Guedes & G. Smagghe, 2015. Lethal and sublethal effects of azadirachtin on the bumblebee Bombus terrestris (Hymenoptera: Apidae). Ecotoxicology, 24 (1): 130-142.
• Bensebaa, F., S. Kilani-Morakchi, N. Aribi & N. Soltani, 2015. Evaluation of pyriproxyfen, a juvenile hormone analog, on Drosophila melanogaster (Diptera: Drosophilidae) insecticidal activity, ecdysteroid contents and cuticle formation. European Journal of Entomology, 112 (4): 625-631.
• Bernardes, R. C., H. V. V. Tomé, W. F. Barbosa, R. N. C. Guedes & M. A. P. Lima, 2017. Azadirachtin-induced antifeeding in neotropical stingless bees. Apidologie, 48 (3): 275-285.
• Bezzar-Bendjazia, R., S. Kilani-Morakchi, M. Ferdenache & N. Aribi, 2017. Azadirachtin induces larval avoidance and antifeeding by disruption of food intake and digestive enzymes in Drosophila melanogaster (Diptera: Drosophilidae). Pesticide Biochemistry and Physiology, 143 (1): 135-140.
• Çelik, D., R. Özbek & F. Uçkan, 2017. Effects of indole-3-acetic acid on hemocytes of Achroia grisella Fabr. (Lepidoptera: Pyralidae). Journal of the Entomological Research Society, 19 (2): 83-93.
• Chaudhary, S., R. K. Kanwar, A. Sehgal, D. M. Cahill, C. J. Barrow, R. Sehgal & J. R. Kanwar, 2017. Progress on Azadirachta indica based biopesticides in replacing synthetic toxic pesticides. Frontiers in Plant Science, 8 (1): 610-623.
• Dorrah, M. A., A. A. Mohamed & E. H. Shaurub, 2019. Immunosuppressive effects of the limonoid azadirachtin, insights on a nongenotoxic stress botanical, in flesh flies. Pesticide Biochemistry and Physiology, 153 (1): 55-66.
• Duarte, J. P., L. R. Redaelli, C. E. Silva & S. M. Jahnke, 2020. Effect of Azadirachta indica (Sapindales: Meliaceae) Oil on the Immune System of Spodoptera frugiperda (Lepidoptera: Noctuidae) Immatures. Journal of Insect Science, 20 (3): 1-6.
• Eleftherianos, I., C. Heryanto, T. Bassal, W. Zhang, G. Tettamanti & A. Mohamed, 2021. Haemocyte-mediated immunity in insects: Cells, processes and associated components in the fight against pathogens and parasites. Immunology, 164 (3): 401-432.
• Er, A. & M. Keskin, 2016. Influence of abscisic acid on the biology and hemocytes of the model insect Galleria mellonella (Lepidoptera: Pyralidae). Annals of the Entomological Society of America, 109 (2): 244-251.
• Er, A., D. Taşkıran & O. Sak, 2017. Azadirachtin induced effects on various life history traits and cellular immune reactions of Galleria mellonella (Lepidoptera: Pyralidae). Archives of Biological Science, 69 (2): 335-344.
• Er, A., F. Uçkan, D. B. Rivers, E. Ergin & O. Sak, 2009. Effects of parasitization and envenomation by the endoparasitic wasp Pimpla turionellae (Hymenoptera: Ichneumonidae) on hemocyte numbers, morphology, and viability of its host Galleria mellonella (Lepidoptera: Pyralidae). Annals of the Entomological Society of America, 103 (2): 273-282.
• Ferdenache, M., R. Bezzar-Bendjezia, F. Marion Poll & S. Kilani-Morakchi, 2019. Transgenerational effects from single larval exposure to azadirachtin on life history and behavior traits of Drosophila melanogaster. Scientific Reports 9 (1):17015.
• Gardiner, E. M. M. & M. R. Strand, 2000. Hematopoiesis in larval Pseudoplusia includens and Spodoptera frugiperda. Archives of Insect Biochemistry, 43 (4):147-164.
• Gontijo, L. M., D. Celestino, O. S. Queiroz, R. N. C. Guedes & M. Picanço, 2015. Impacts of azadirachtin and chlorantraniliprole on the developmental stages of pirate bug predators (Hemiptera: Anthocoridae) of the tomato pinworm Tuta absoluta (Lepidoptera: Gelechiidae). Florida Entomologist, 98 (1): 59-64.
• Huang, J. F., K. J. Shui, H. Y. Li, M. Y. Hu & G. H. Zhong, 2011. Antiproliferative effect of azadirachtin A on Spodoptera litura Sl-1 cell line through cell cycle arrest and apoptosis induced by up-regulation of p53. Pesticide Biochemistry and Physiology, 99 (1): 16-24.
• Isman, M. B., 2006. Botanical insecticides, deterrents, and repellents in modern agriculture and an increasingly regulated world. Annual Review of Entomology, 51 (1): 45-66.
• Jagannadh, V. & V. S. K. Nair, 1992. Azadirachtin-induced effects on larval-pupal transformation of Spodoptera mauritra. Physiological Entomology, 17 (1): 56-61.
• Kaya, S., G. Akkuş, S. Türkdoğan & B. Gündüz, 2021. Influence of Helichrysum arenarium on hemocyte-mediated immune responses and phenoloxidase enzyme activity of model organism Galleria mellonella (L.). International Journal of Tropical Insect Science, 41 (4): 2521-2528.
• Kilani-Morakchi, S., H. Morakchi-Goudjil & K. Sifi, 2021. Azadirachtin-based insecticide: Overview, risk assessments, and future directions. Frontiers in Agronomy, 3 (1): 1-13.
• Konecka, E., A. Kaznowski & D. Tomkowiak, 2019. Insecticidal activity of mixtures of Bacillus thuringiensis crystals with plant oils of Sinapis alba and Azadirachta indica. Annals of Applied Biology, 174 (3): 364-371.
• Lai, D., X. Jin, H. Wang, M. Yuan & H. Xu, 2014. Gene expression profile change and growth inhibition in Drosophila larvae treated with azadirachtin. Journal of Biotechnology, 185 (1): 51-56.
• Lavine, M. D. & M. R. Strand, 2002. Insect hemocytes and their role in immunity. Insect Biochemistry and Molecular Biology, 32 (10): 1295-1309.
• Li, X. D., W. K. Chen & M. Y. Hu, 1995. Studies on the effects and mechanisms of azadirachtin and rhodojaponin on Spodoptera litura (F.). Journal of South China Agricultural University, 16 (2): 80-85.
• Liu, P. F., W. Wang, X. Ling, Q, Lu, J. Zhang, R. He & C. Hang, 2019. Regulation hormone-related genes in Ericerus pela (Hemiptera: Coccidae) for dimorphic metamorphosis. Journal of Insect Science, 19 (5): 16-25.
• Mordue, A. J., 2004. “Present Concepts of the Mode of Action of Azadirachtin from Neem, 229-257”. In: Neem: Today and in the New Millennium (Eds. O. Koul & S. Wahab). Springer Dordrecht, The Netherlands, 276 pp.
• Mordue, A. J., E. D. Morgan & A. J. Nisbet, 2005. “Azadirachtin, A Natural Product in Insect Control, 117-135”. In: Comprehensive Molecular Insect Science (Eds. L. I. Gilbert, K. Iatrou & S. S. Gill). Elsevier Oxford, 459 pp.
• Nunes, C., E. Sucena & T. Koyama, 2021. Endocrine regulation of immunity in insects. The FEBS Journal, 288 (1): 3928-3947.
• Okumu, F. O., B. G. J. Knols & U. Fillinger, 2007. Larvicidal effects of a neem (Azadirachta indica) oil formulation on the malaria vector Anopheles gambiae. Malaria Journal, 6 (1): 63-70.
• Pandey, J. P. & R. K. Tiwari, 2011. Neem based insecticides interaction with development and fecundity of red cotton bug, Dysdercus cingulatus Fab. International Journal of Agricultural Research, 6 (4): 335-346.
• Pandey, J. P., R. K. Tiwari & D. Kumar, 2008. Reduction in haemocyte mediated immune response in Danais chrysippus following treatment with neem-based insecticides. Journal of Entomology, 5 (3): 200-206.
• Qin, D., P. Zhang, Y. Zhou, B. Liu, C. Xiao, W. Chen & Z. Zhang, 2020. Antifeeding effects of azadirachtin on the fifth instar Spodoptera litura larvae and the analysis of azadirachtin on target sensilla around mouthparts. Archives of Insect Biochemistry and Physiology, 103 (4): e21646.
• Rajak, P., M. Dutta & S. Roy, 2015. Altered differential hemocyte count in 3rd instar larvae of Drosophila melanogaster as a response to chronic exposure of Acephate. Interdisciplinary Toxicology, 8 (2): 84-88.
• Salehzadeh, A., A. Akhkha, W. Cushley, R. L. Adams, J. R. Kusel & R. H. Strang, 2003. The antimitotic effect of the neem terpenoid azadirachtin on cultured insect cells. Insect Biochemistry and Molecular Biology, 33 (7): 681-689.
• Schmutterer, H. & R. P. Singh, 1995. “List of Insect Pests Susceptible to Neem Products, 326-365”. In: The Neem Tree: Azadirachta indica A. Juss. and other Meliaceae plants (Ed. H. Schmutterer). VCH Weinheim, 696 pp.
• Scudeler, E. L. & D. C. dos Santos, 2013. Effects of neem oil (Azadirachta indica A. Juss) on midgut cells of predatory larvae Ceraeochrysa claveri (Navás, 1911) (Neuroptera: Chrysopidae). Micron, 44 (1): 125-132.
• Sharma, P., A. B. Jha, R. S. Dubey & M. Pessarakli, 2012. Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. Journal of Botany, 217037 (1): 1-26.
• Sharma, P. R., B. P. Sharma & B. P. Saxena, 2003. Effects of neemgold on haemocytes of the tobacco armyworm, Spodoptera litura (Fabr.) (Lepidoptera: Noctuidae). Current Science, 84 (5): 690-695.
• Shu, B., H. Yu, Y. Li, H. Zhong, X. Li, L. Cao & J. Lin, 2021. Identification of azadirachtin responsive genes in Spodoptera frugiperda larvae based on RNA- seq. Pesticide Biochemistry and Physiology, 172 (1): 104745.
• Silva, M. A., G. C. D. Bezerra-Silva, J. D. Vendramim & T. Mastrangelo, 2013. Sublethal effect of neem extract on mediterranean fruit fly adults. Revista Brasileira de Fruticultura, 35 (1): 93-101.
• Silva, C. T. S., V. Wanderley-Teixeira, G. Cruz, F. M. Cunha & A. Teixeira, 2020. Immune and nutritional responses of Podisus nigrispinus (Hemiptera: Pentatomidae) nymphs sprayed with azadirachtin. Austral Entomology, 59 (1): 215-224.
• Sun, R., G. Cui, Y. Chen, B. Shu, G. Zhong & X. Yi, 2018. Proteomic profiling analysis of male infertility in Spodoptera litura larvae challenged with azadirachtin and its potential regulated pathways in the following stages. Proteomics, 18 (19): e1800192.
• Tunca, H., N. Kılınçer & C. Özkan, 2012. Side-effects of some botanical insecticides and extracts on the parasitoid, Venturia canescens (Grav.) (Hymenoptera: Ichneumonidae). Türk Entomoloji Dergisi, 36 (2): 205-214.
• Uçkan, F., İ. Haftacı & E. Ergin, 2011. Effects of indol-3-acetic acid on biological parameters of the larval endoparasitoid Apanteles galleriae (Hymenoptera: Braconidae). Annals of the Entomological Society of America, 104 (1): 77-82.
• Vilca Malqui, K. S., J. L. Vieira, R. N. C. Guedes & L. M. Gontijo, 2014. Azadirachtin-induced hormesis mediating shift in fecundity longevity trade-off in the Mexican bean weevil (Chrysomelidae: Bruchinae). Journal of Economic Entomology, 107 (2): 860-866.
• Xavier, V. M., D. Message, M. C. Picanço, M. Chediak, P. A. S. Júnior, R. S. Ramos & J. C. Martins, 2015. Toxicity and sublethal effects of botanical insecticides to honey bees. Journal of Insect Science, 15 (1): 137-142.
• Zhao, T., D. Lai, Y. Zhou, H. Xu, Z. Zhang, S. Kuang & X. Shao, 2019. Azadirachtin A inhibits the growth and development of Bactrocera dorsalis larvae by releasing cathepsin in the midgut. Ecotoxicology and Environmental Safety, 183 (1): 109512.
• Zhong, B., C. Lv & W. Qin, 2017. Effectiveness of botanical insecticide azadirachtin against Tirathaba rufivena (Lepidoptera: Pyralidae). Florida Entomologist, 100 (2): 215-218.
• Zibaee, A. & A. R. Bandani, 2010. Effects of Artemisia annua L. (Asteracea) on the digestive enzymatic profiles and the cellular immune reactions of the Sunn pest, Eurygaster integriceps (Heteroptera: Scutelleridae), against Beauveria bassiana. Bulletin of Entomological Research, 100 (2): 185-196.
• Zibaee, A., A. R. Bandani & D. Malagoli, 2012. Methoxyfenozide and pyriproxifen alter the cellular immune reactions of Eurygaster integriceps Puton (Hemiptera: Scutelleridae) against Beauveria bassiana. Pesticide Biochemistry and Physiology, 102 (1): 30-37.