Korean journal of applied entomology (한국응용곤충학회지)

Korean Society of Applied Entomology (한국응용곤충학회)
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A Review on the Insecticidal Activity of Neem Extracts (Azadirachtin) and its Current Status of Practical use in Korea

님추출물 아자디라크틴의 살충활성과 국내 이용현황에 대한 고찰

  • Kim, Dong-soon (Majors in Plant Resource Sciences & Environment, College of Applied Life Science, SARI, Jeju National University)
  • 김동순 (제주대학교 생명자원과학대학(SARI))
  • Received : 2021.09.15
  • Accepted : 2021.11.23
  • Published : 2021.12.01
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Abstract

As a tropical plant, the neem tree (Azadirachta indica) has been used for a long time for disease and pest control and medical purposes. In this paper, we reviewed for the active ingredient of neem, the mode of action of azadirachtin in terms of insect growth regulation, repellent, feeding inhibition and oviposition against plant pests. And also we reviewed the current status of practical use in Korea. Among 57 products of neem-based eco-friendly organic agricultural materials distributed in Korea, seven products were certified for their efficacy. The average azadirachtin content of the seven products was 0.38%, which was 5.5 times less than the average content of 2.1% distributed worldwide. In the control effect on neem products in Korea, it showed some variation on aphids, but most showed a control effect of more than 90%. The treatment effects of Lycorma delicatula nymphs were 73-77%, and the control effects for thrips were obtained in the range of 50-72% mortality. The mortality effects against bug and moth species were generally low. It is expected that this review would provide important information necessary for the understanding of distributed neem products and the interpretation of experimental data.

열대식물인 인도멀구슬나무(Azadirachta indica)는 병해충과 방제와 의학적인 목적으로 오랫동안 이용하였다. 본고에서는 님제의 활성성분인 아자디라크틴의 해충에 대한 곤충생장조절, 기피, 섭식저해, 산란억제 등 다양한 작용기작과 국내 이용현황에 대하여 고찰하였다. 국내 유통되는 친환경유기농자재 중에서 님제 제품은 총 57종이었다. 그중 효능효과가 표시된 자재는 7종이었고 평균 아자디라크틴 함량은 0.38%로써 세계적으로 유통되는 평균 함량 2.1%와 비교할 때 약 5.5배 낮았다. 국내에서 님제의 방제효과에서 진딧물은 실험에서 다소 변이는 있었으나 대부분 90% 이상의 방제효과를 보였다. 꽃매미 약충에 누적살충률은 73~77%를 보였고, 총채벌레에 대한 방제가는 50~72% 범위로 살포효과가 인정되었다. 노린재와 나방류에 대한 방제효과는 대체적으로 낮았다. 본고는 유통되는 님제품의 이해와 실험자료의 해석에 필요한 주요한 정보를 제공해줄 수 있을 것으로 기대된다.

Keywords

Acknowledgement

This work was supported by the 2021 education, research and student guidance grant funded by Jeju National University. We are grateful to Sustainable Agriculture Research Institute (SARI) in Jeju National University for providing the experimental facilities.

References

  1. Agbo, B.E., Nta, A.I., Ajaba, M.O., 2015. A review on the use of neem (Azadirachta indica) as a biopesticide. J. Bio-pestic. Environ. 2, 58-65.
  2. Agbo, B.E., Nta, A.I., Ajaba, M.O., 2019. Bio-pesticidal properties of neem (Azadirachta indica). Adv. Trends. Agric. Sci. 1, 17-26.
  3. Akhtar, M., 2000. Nematicidal potential of the neem tree Azadirachta indica (A. Juss). Integr. Pest Manag. Rev. 5, 57-66. https://doi.org/10.1023/a:1009609931223
  4. Amaral, K.D., Martinez, L.C., Lima, M.A.P., Serrao, J.E., Castro Della Lucia, T.M., 2018. Azadirachtin impairs egg production in Atta sexdens leaf-cutting queens. Environ. Pollut. 243, 809-814. https://doi.org/10.1016/j.envpol.2018.09.066
  5. AMR (Allied Market Research),2021. Neem extract market by application (agriculture, personal care products, pharmaceutical, animal feed): Global opportunity analysis and industry forecast, 2015-2022. https://www.alliedmarketresearch.com/neem-extractmarket. (accessed on 12 November, 2021).
  6. Anuradha, A., Annadurai, R.S., Shashidhara, L.S., 2007. Actin cytoskeleton as a putative target of the neem limonoid azadirachtin A. Insect. Biochem. Mol. Biol. 37, 627-634. https://doi.org/10.1016/j.ibmb.2007.03.009
  7. Asogwa, E.U., Ndubuaku, T.C.N., Ugwu, J.A. Awe, O.O., 2010. Prospects of botanical pesticides from neem, Azadirachta indica for routine protection of cocoa farms against the brown cocoa mirid - Sahlbergella singularis in Nigeria. J. Med. Plant. Res. 4, 1-6. https://doi.org/10.3923/rjmp.2010.1.13
  8. Benuzzi, M., Ladurner, E., 2018. Plant protection tools in organic farming, in Handbook of Pest Management in Organic Farming, in: Vacante, V., Kreiter, S. (Cesena, FC: CAB international) (Eds), 24-59.
  9. Bezzar-Bendjazia, R., Kilani-Morakchi, S., Ferdenache, M., Aribi, N., 2017. Azadirachtin induces larval avoidance and antifeeding by disruption of food intake and digestive enzymes in Drosophila melanogaster (Diptera: Drosophilidae). Pestic. Biochem. Physiol. 143, 135-140. https://doi.org/10.1016/j.pestbp.2017.08.006
  10. 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. Afr. Entomol. 23, 224-233. https://doi.org/10.4001/003.023.0104
  11. Broughton, H.B., Ley, S.V., Slawin, M.Z., Williams, D.J., Morgan, E.D., 1986. X-ray crystallographic structure determination of detigloyldihydroazadirachtin and reassignment of structure of the limonoid insect antifeedant azadirachtin. J. Chem. Soc. Commun. 46-47
  12. Butterworth, J.H., Morgan, E.D., 1968. Isolation of a substance that suppresses feeding in locusts. J. Chem. Soc. Chem. Commun. 23-24.
  13. Butterworth, J.H., Morgan, E.D., Percy, G.R., 1972. The structure of azadirachtin; the functional groups. J. Chem. Soc. Perkin Trans. 1, 2445-2450. https://doi.org/10.1039/p19720002445
  14. Caldwell, B., Rosen, E.B., Sideman, E., Shelton, A.M., Smart, C.D., 2013. Resource guide for organic insect and disease management. New York State Agricultural Experiment Station. Arnold Printing Corp, Ithaca, New York, p. 202.
  15. Chaudhary, S., Kanwar, R.K., Sehgal, A., Cahill, D.M., Barrow, C.J., Sehgal, R., Kanwar, J.R., 2017. Progress on Azadirachta indica based biopesticides in replacing synthetic toxic pesticides. Front. Plant Sci. 8, 610. doi: 10.3389/fpls.2017.0061.
  16. Chopra, R., 1928. Annual report of the entomologist to the government, Punjab, 1925-26. Rep. Dep. Agric. Punjab 2, 67-125.
  17. Delventhal, R., Carlson, J., 2016. Bitter taste receptors confer diverse functions to neurons. eLife 5, e11181. doi: 10.7554/eLife.11181.
  18. Dorn, A., Rademacher, J.M., Sehn, E., 1987. Effects of azadirachtin on reproductive organs and fertility in the large milkweed bug, Oncopeltus fasciatus. Proc. 3rd Int. Neem Conf., pp. 273-288.
  19. Dubrovsky, E.B., 2005. Hormonal cross talk in insect development. Trends Endocrinol. Metab. 16, 6-11. https://doi.org/10.1016/j.tem.2004.11.003
  20. Er, A., Taskiran, D., Sak, O., 2017. Azadirachtin-induced effects on various life history traits and cellular immune reactions of Galleria mellonella (Lepidoptera: Pyralidae). Arch. Biol. Sci. 69, 335-344. https://doi.org/10.2298/ABS160421108E
  21. Ermel, K., Pahlich, E., Schmutterer, H., 1987. Azadirachtin content of neem kernels from different geographical locations and its dependence on temperature, relative humidity and light, in: Schmutterer, H., Ascher, K.R.S. (Eds.), Natural pesticides from the neem tree (Azadiracltta indica A Juss) and other tropical plants. Eschborn: GTZ. pp. 171-184.
  22. Fer, P., Leupolz, W., Quentin, H., Praneetvatakul, S., Varela, A., 2000. Case studies of neem processing projects assisted by GTZ in Kenya, Dominican Republic, Thailand and Nicaragua. GTZ Report in 2000, Deutsche Gesellschaft fur Technische Zusammenarbeit, Germany, p. 152. http://www.nzdl.org/cgi-bin/library (accessed on 30 August, 2021).
  23. Garcia, E.S., Luz, N., Azambuja, P., Rembold, H., 1990. Azadirachtin depresses the release of prothoracicotropic hormone in Rhodnius prolixus larvae: evidence from head transplantations. J. Insect. Physiol. 36, 679-682. https://doi.org/10.1016/0022-1910(90)90073-O
  24. Ghazawi, N.A., El-Shranoubi, E.D., El-Shazly, M.M., Abdel Rahman, K.M., 2007. Effects of azadirachtin on mortality rate and reproductive system of the grasshopper Heteracris littoralis Ramb (Orthoptera: Acrididae). J. Orthopt. Res. 16, 57-65. https://doi.org/10.1665/1082-6467(2007)16[57:EOAOMR]2.0.CO;2
  25. Ghazawy, N.A., Awad, H.H., Abdel Rahman, K.M., 2010. Effects of azadirachtin on embryological development of the desert locust Schistocerca gregaria Forskal (Orthoptera: Acrididae). J. Orthoptera Res. 19, 327-332. https://doi.org/10.1665/034.019.0220
  26. Govindchari, T.R., 1992. Chemistry and biological investigation on Azadirachta indica (the neem tree). Curr. Sci. 63, 117-122.
  27. Grant, I.F., Tirol, A.C., Aziz, T., Watanabe, I., 1983. Regulation of invertebr grazers to enhance biomass and nitrogen fixation of cyanophyceae in Wetland rice field. J. Soil Sci. Soc. Am. 47, 669-675. https://doi.org/10.2136/sssaj1983.03615995004700040013x
  28. Grdisa, M., Grsic, K., 2013. Botanical insecticides in plant protection. Agric. Cons. Sci. 78, 85-93.
  29. Han, S.-B., Kim, J.-H., 2013. Research trend of neem based biopesticides. Korean J. Pestic. Sci. 17, 220-230. https://doi.org/10.7585/kjps.2013.17.3.220
  30. Hasan, F., Ansari, M.S., 2011. Toxic effects of neem-based insecticides on Pieris brassicae (Linn.). Crop Prot. 30, 502-507. https://doi.org/10.1016/j.cropro.2010.11.029
  31. Hummel, H.E., Langner, S., Hein, D.F., Sanguanpong, U., Schmutterer, H., 2016. Unusually versatile plant genus Azadirachta with many useful and so far incompletely exploited properties for agriculture, medicine and industry. Acta. Fytotechn. Zootechn. 18, 169-175.
  32. Isman, M.B., 2006. Botanical insecticides, deterrents, and repellents in modern agriculture and an increasingly regulated world. Annu. Rev. Entomol. 51, 45-66. https://doi.org/10.1146/annurev.ento.51.110104.151146
  33. Jacobson, M., 1986. The neem tree: Natural resistance par excellence. Am. Chem. Soc. Symp. Ser. 296, 220-232.
  34. Kabeh, J.D., Jalingo, M.G.D.S.S., 2007. Exploiting neem (Azadirachta Indica) resources for improving the quality of life in Taraba State, Nigeria. Int. J. Agri. Biol. 9, 530-532.
  35. Ketkar, C.M., 1983. Crop experiments to increase the efficacy of urea fertilizer nitrogen by neem by-products. Proc. 2nd Int. Neem Conf. Germany, pp. 507-518.
  36. Khater, H.F., 2012. Prospects of botanical biopesticides in insect pest management. Pharmacologia 3, 641-656. https://doi.org/10.5567/pharmacologia.2012.641.656
  37. Khosravi, R., Sendi, J.J., 2013. Effect of neem pesticide (achook) on midgut enzymatic activities and selected biological compounds in the hemolymph of lesser mulberry pyralid, Glyphodes pyloalis walker (Lepidoptera: Pyralidae). J. Plant. Prot. Res. 5, 238-247. https://doi.org/10.2478/jppr-2013-0036
  38. Kilani-Morakchi, S., Morakchi-Goudjil, H., Sifi, K., 2021. Azadira chtin-based insecticide: overview, risk assessments, and future directions. Front. Agron. 3, 676208. doi: 10.3389/fagro.2021.676208.
  39. Krauss, W., Baumann, S., Bokel, M., Keller, U., Klenk, A., Klingele, M., Pohnl, H., Schwinger, M., 1987. Control of insect feeding and development by constituent Melia azadirach and Azadirachta indica, in: Schmutterer, H., Ascher, K.R.S. (Eds.), Natural pesticides from the Neem tree and other tropical plants, Proc. 3rd Int. Neem Conf. GIZ, Eschborn, Germany. pp. 111-125.
  40. Kumar, B.R., 2021. SR Neem Agro Products, India. https://www.exportersindia.com/s-r-neem-agro-products (accessed on 30 August, 2021).
  41. Lai, D., Jin, X., Wang, H., Yuan, M., Xu, H., 2014. Gene expression profile change and growth inhibition in Drosophila larvae treated with azadirachtin. Biotechnol. 185, 51-56.
  42. Lee, Y., Kim, S., Montell, C., 2010. Avoiding DEET through insect gustatory receptors. Neuron 67, 555-561. https://doi.org/10.1016/j.neuron.2010.07.006
  43. Liu, P.F., Wang, W., Ling, X., Lu, Q., Zhang, J., He, R., Hang, C., 2019. Regulation hormone-related genes in Ericerus pela (Hemiptera: Coccidae) for dimorphic metamorphosis. J. Insect Sci. 19, 16. doi: 10.1093/jisesa/iez092.
  44. Maia, M.F., Moore, S.J., 2011. Plant-based insect repellents: a review of their efficacy, development and testing. Malar. J. 10 (Suppl. 1), S11. https://doi.org/10.1186/1475-2875-10-S1-S11
  45. Marco, M.P., Pascual, N., Belles, X., Camps, F., Messeguer, A., 1990. Ecdysteroid depletion by azadirachtin in Tenebrio molitor pupae. Pest. Biochem. Physiol. 38, 60-65. https://doi.org/10.1016/0048-3575(90)90149-V
  46. Mitchell, M.J., Smith, S.L., Johnson, S., Morgan, E.D., 1997. Effects of the neem tree compounds azadirachtin, salannin, nimbin, and 6-desacetylnimbin on ecdysone 20-monooxygenase activity. Arch. Insect Biochem. Physiol. 35, 199-209. https://doi.org/10.1002/(SICI)1520-6327(1997)35:1/2<199::AID-ARCH18>3.0.CO;2-6
  47. Moga, M.A., Balan, A., Anastasiu, C.V., Dimienescu, O.G., Neculoiu, C.D., Gavris, C., 2018. An overview on the anticancer activity of Azadirachta indica (neem) in gynecological cancers. Int. J. Mol. Sci. 19, 3898. doi: 10.3390/ijms19123898.
  48. Mordue, A.J., Blackwell, A., 1993. Azadirachtin: an update. J. Insect Physiol. 39, 903-924. https://doi.org/10.1016/0022-1910(93)90001-8
  49. Mordue, A.J., Morgan, E.D., Nisbet, A.J., 2010. Azadirachtin, a natural product in insect control, in: Gilbert, L.I., Gill, S.S. (Eds.), Insect Control: Biological and synthetic agents, Elsevier Academic. pp. 185-203.
  50. Mordue, A.J., Nisbet, A.J., 2000. Azadirachtin from the neem tree Azadirachta indica: its action against insects. Anais da Sociedade Entomologica do Brasil, 4, 615-632.
  51. Morgan, E.D., 1981. Strategy in the isolation of insect control substances from plants, in: Schmutterer, H., Ascher, K.R.S., Rembold, H. (Eds.), Natural pesticides from the neem tree (Azadirachta indica A Juss), Eschborn: GTZ. pp. 43-52.
  52. Morgan, E.D., 2009. Azadirachtin, a scientific gold mine. Bioorg. Med. Chem. 17, 4096-4105. https://doi.org/10.1016/j.bmc.2008.11.081
  53. NPCS (NIIR PROJECT CONSULTANCY SERVICES),2015. Market survey cum detailed thechno economic feasibility report on neem plantation and processing product. NPCS/2845/23076, OP: BCCACA RP: OS-1. Delhi, India.
  54. Oulhaci, M.C., Denis, B., Kilani-Morakchi, S., Sandoz, J.C., Kaiser, L., Joly, D., Aribi, N., 2018. Azadirachtin effects on mating success, gametic abnormalities and progeny survival in Drosophila melanogaster (Diptera). Pest Manag. Sci. 74, 174-180. https://doi.org/10.1002/ps.4678
  55. Pankaj, S., Lokeshwar, T., Mukesh, B., Vishnu, B., 2011. Review on neem (Azadirachta indica): Thousand problems on solution. Int. Res. J. Pharm. 2, 97-102. https://doi.org/10.7897/2230-8407.04919
  56. Paranagama, P.A., Connolly, J.D., Strang, R.H.C., 2004. Azadirachtin effects on proteins synthesized in fat body, haemolymph, ovary and midgut of locusts, Schistocerca gregaria. J. Natl. Sci. Fond. 32, 13-28.
  57. Premachandra, D.W., Borgemeister, C., Poehling, H.M., 2005. Effects of neem and spinosad on Ceratothripoides claratris (Thysanoptera: Thripidae), an important vegetable pest in Thailand, under laboratory and greenhouse conditions. J. Econ. Entomol. 98, 438-48. https://doi.org/10.1603/0022-0493-98.2.438
  58. Qiao, J., Zou, X., Lai,D., Yan, Y., Wang, Q., Li, W., Deng, S., Xu, H., Gu, H., 2014. Azadirachtin blocks the calcium channel and modulates the cholinergic miniature synaptic current in the central nervous system of Drosophila. Pest. Manag. Sci. 70, 1041-1047. https://doi.org/10.1002/ps.3644
  59. Rembold, H., Forster, H., Czoppelt, C.H., 1987a. Structure and biological activity of azadirachtins A and B, in: Schmutterer, H., Ascher, K.R.S. (Eds.), Natural pesticides from the neem tree (Azadirachta indica A Juss) and other tropical plants. Eschbom: GTZ. pp. 149-160.
  60. Rembold, H., Forster, H., Sonnenbichler, J., 1987b. Structure of azadirachtin B. Z. Naturforsch C 42, 4-6. https://doi.org/10.1515/znc-1987-1-202
  61. Rembold, H., Forster, I.I., Czoppelt, Ch., Rao, P.J., Sieber, K.P., 1984 The azadirachtins, a group of insect growth regulators from the neem tree, in: Natural pesticides from the neem tree (Azadirachta indica A Juss) and other tropical plants Schmutterer, H., Ascher, K.R.S. (Eds.), Eschbom: GTZ. pp. 153-162.
  62. Rembold, H., Sieber, K.P., 1981. Inhibition of oogenesis and ovarian ecdysteroid synthesis by azadirachtin in Locusta migratoria migratorioides (R. and F.). Z. Naturforsch. C 36, 466-469. https://doi.org/10.1515/znc-1981-5-621
  63. Rembold, H., Uhl, M., Miiller, T.H., 1987c. Effect of azadirachtin A on hormonal titres during the gonadotrophic cycle of Locust migratoria, in: Schmutterer, H., Ascher, K.R.S. (Eds.), Natural pesticides from the neem tree (Azadirachta indica A Juss) and other tropical plants, Eschborn: GTZ. pp. 289-298.
  64. Riedl, S.J., Shi, Y., 2004. Molecular mechanisms of caspase regulation during apoptosis. Nat. Rev. Mol. Cell Biol. 5, 897-907. https://doi.org/10.1038/nrm1496
  65. Roberston, S.L., Ni, W., Dhadialla, T.S., Nisbet, A.J., Mc Custer, C., Ley, S.V., Mordue, W., Mordue 'Luntz' A.J., 2007. Identification of a putative azadirachtin-binding complex from Drosophila Kc167 cells. Arch. Insect Biochem. Physiol. 64, 200-208. https://doi.org/10.1002/arch.20171
  66. Salehzadeh, A., Jabbar, A., Jennens, L., Ley, S.V., Annadurai, R.S., Adams, R., Strang, R.H.C., 2002. The effects of phytochemical pesticides on the growth of cultured invertebrate and vertebrate cells. Pest Manag. Sci. 58, 268-276. https://doi.org/10.1002/ps.449
  67. Schmutterer, H., 1990. Properties and potential of natural pesticides form the neem tree, Azadirachta indica. Ann. Rev. Entomol. 35, 271-297. https://doi.org/10.1146/annurev.en.35.010190.001415
  68. Schmutterer, H., Singh, R.P., 1995. List of insects susceptible to neem products, in: Schmutterer, H. (Ed.), The Neem Tree Azadirachta indica A. Juss. and other Meliaceae Plants. Wiley-VCH, New York. pp. 326-365.
  69. Shannag, H.K., Capinera, J.L., Freihat, N.M., 2015. Effects of neem-based insecticides on consumption and utilization of food in larvae of Spodoptera eridania (Lepidoptera: Noctuidae). J. Insect Sci. 15, 152. doi: 10.1093/jisesa/iev134.
  70. Shu, B., Wang, W., Hu, Q., Huang, J., Hu, M., Zhong, G., 2015. A comprehensive study on apoptosis induction by azadirachtin in Spodoptera frugiperda cultured cell line Sf9. Arch. Insect. Biochem. Physiol. 89, 153-168. https://doi.org/10.1002/arch.21233
  71. Shu, B., Yu, H., Li, Y., Zhong, H., Li, X., Cao, L., Lin, J., 2021. Identification of azadirachtin responsive genes in Spodoptera frugiperda larvae based on RNAseq. Pest. Biochem. Physiol. 172, 104745. https://doi.org/10.1016/j.pestbp.2020.104745
  72. Smith, S.L., Mitchell, M.J., 1988. Effects of azadirachtin on insect cytochrome P-450 dependent ecdysone 20-monooxygenase activity. Biochem. Biophys. Res. Commun. 154, 559-563. https://doi.org/10.1016/0006-291X(88)90176-3
  73. Stark, J.D., Walter, J.F., 1995. Neem oil and neem oil components affect the efficacy of commercial neem insecticides. J. Agric. Food Chem. 43, 507-512. https://doi.org/10.1021/jf00050a047
  74. Subrahmanyan, B., 1990. Azadirachtin: A naturally occurring insect growth regulator. Proc. Indian Acad. Sci. (Anim. Sci.), 99, 277-288. https://doi.org/10.1007/BF03186397
  75. Sun, R., Cui, G., Chen, Y., Shu, B., Zhong, G., Yi, X., 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, e1800192. doi:10.1002/pmic.201800192.
  76. Tennessen, J.M., Thummel, C.S., 2011. Coordinating growth and maturation insights from Drosophila. Curr. Biol. 21, 750-757.
  77. Thoeming, G., Borgemeister, C., Setamou, M., Poehling, H.M., 2003. Systemic effects of neem on western flower thrips, Frankliniella occidentalis (Thysanoptera: Thripidae). J Econ Entomol. 96, 817-825. https://doi.org/10.1603/0022-0493-96.3.817
  78. Thoeming, G., Poehling, H.-M., 2006. Soil application of different neem products to control Ceratothripoides claratris (Thysanoptera: Thripidae (on tomatoes grown under protected cultivation in the humid tropics. Thai. Int. J. Pest Mana. 52, 239-248. https://doi.org/10.1080/09670870600733774
  79. Tome, H.V.V., Martins, J.C., Correea, S., Galdino, T.V.S., Picancon, M.C., Guedes, R.N. C., 2013. Azadirachtin avoidance by larvae and adult females of the tomato leafminer Tuta absoluta. Crop Prot. 46, 63-69. https://doi.org/10.1016/j.cropro.2012.12.021
  80. Volkonsky, M., 1937. Sur un proccde nouveau de protection des cultures contre Ics acridines. C. R. Soc. Bioi. 125, 417-418.
  81. Weiss, L.A., Dahanukar, A., Kwon, J.Y., Banerjee, D., Carlson, J.R., 2011. The molecular and cellular basis of bitter taste in Drosophila. Neuron 69, 258-272. https://doi.org/10.1016/j.neuron.2011.01.001
  82. Yan, Y., Gu, H., Xu, H., Zhang, Z., 2017. Induction of aversive taste memory by azadirachtin and its effects on dopaminergic neurons of Drosophila. J. South. China Agri. Univ. 38, 12-18.
  83. Zannao, P.R., Miura, I., Nakanishi, K., Elder, D.L., 1975. Structure of insect phagorepellent azadirachtin: applications of PRFT CWD Carbon-13 nuclear magnetic resonance. J. Am. Chem. Soc. 97, 1975-1977. https://doi.org/10.1021/ja00840a073
  84. Zhao, J., Zhou, Y., Li, X., Cai, W., Hua, H., 2017. Silencing of juvenile hormone epoxide hydrolase gene (Nljheh) enhances short wing formation in a macropterous strain of the brown planthopper, Nilaparvata lugens. J. Insect Physiol. 102, 18-26. https://doi.org/10.1016/j.jinsphys.2017.08.012