اثرات سمی پنیرباد بر فیزیولوژی کرم غوزه‌ی پنبه Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae)

نوع مقاله : مقاله کامل، انگلیسی

نویسندگان

گروه گیاهپزشکی، دانشکده علوم کشاورزی، دانشگاه گیلان، رشت، ایران

10.61186/jesi.44.3.1

چکیده

کرم غوزه‌ی پنبه Helicoverpa armigera (Hübner) یکی از مهم‌ترین آفات سبزیجات در سراسر جهان به شمار می‌رود. امروزه معمولاً اقدامات ایمن جایگزین برای مبارزه با حشرات آفت مختلف توصیه می‌شود. در این بررسی، تاثیر عصاره‌ی اتانولی میوه‌ی یک گیاه دارویی به نام پنیرباد Withania somnifera L. (Solanaceae) علیه لارو سن سوم کرم غوزه‌ی پنبه بررسی گردید. مقادیر LC50، LC30 و LC10 به صورت گوارشی در رژیم غذایی 1/33، 0/53 و 0/14 (% w/v) برآورد شد. بعداً، مقدار LC30 (0/53 % w/v) به دست آمده مجدداً بر روی لاروهای تیمار شده به دلیل تأثیر آن بر برخی مولکول‌ها و آنزیم‌های مهم انجام شد. نتایج حاکی از افزایش میزان اسید اوریک و افزایش فعالیت اسید فسفاتاز، آسپارتات آمینوترانسفراز، لاکتات دهیدروژناز، گلوتاتیون اس-ترانسفراز در مقایسه با گروه شاهد (تغذیه با رژیم غذایی مصنوعی با اتانول به تنهایی) بود. با این حال، فعالیت آلانین آمینوترانسفراز، آلکالین فسفاتاز، کاتالاز، استیل کولین استراز، سوپراکسید دیسموتاز و پراکسیداز کاهش یافت. بافت‌شناسی معده‌ی میانی اختلال در  سلول‌های اپیتلیال اصلی معده میانی و همچنین سایر انواع سلول‌ها را در گروه تیمار در مقابل شاهد نشان داد. اجزای شیمیایی عصاره‌ی اتانولی میوه‌های پنیرباد نیز با استفاده از GC-MS شناسایی شد که اجزای اصلی آن شامل 5-Hydroxymethylfurfural (51/18 درصد) و 4H-Pyran-4-one, 2,3-dihydro-3,5-dihydroxy-6-methyl (21/86 درصد) بود. نتایج ما حاکی از یک محصول طبیعی امیدوارکننده است که می‌تواند به عنوان منبع جدیدی برای کنترل حشرات آفت در نظر گرفته شود.

چکیده تصویری

اثرات سمی پنیرباد بر فیزیولوژی کرم غوزه‌ی پنبه  Helicoverpa armigera  (Hübner) (Lepidoptera: Noctuidae)

کلیدواژه‌ها

موضوعات


عنوان مقاله [English]

The toxic effects of Winter Cherry on the physiology of Cotton Bollworm Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae)

نویسندگان [English]

  • Yasaman Ohadi
  • Roya Azizi
  • Jalal Jalali Sendi
Department of Plant Protection, Faculty of Agricultural Sciences, University of Guilan, Rasht, Iran
چکیده [English]

The cotton bollworm, Helicoverpa armigera (Hübner) is considered as one of the most important pests of vegetables worldwide. Nowadays, alternative safe control measures are usually recommended against various insect pests. We investigated the ethanolic extracts of a medicinal plant fruit called winter cherry Withania somnifera L. (Solanaceae) against third instar larvae of cotton bollworm. The LC50, LC30, and LC10 values were estimated by feeding through larval diet at 1.33, 0.53, and 0.14 (% w/v). Later, the LC30 value (0.53 % w/v) obtained was again treated on third instar larvae to find out its sublethal effects on some important molecules and enzymes. The results showed elevated amount of uric acid and also increased activity in acid phosphatase, aspartate aminotransferase, lactate dehydrogenase, glutathione S-transferase in comparison with the controls (fed artificial diet with ethanol alone). However, decreased activity of alanine aminotransferase, alkaline phosphatase, catalase, acetylcholinesterase, superoxide dismutase, and peroxidase were observed. The midgut histology showed disruption in main midgut epithelial cells as well as other cell types in treated vs controls. Chemical components of the ethanolic extract of winter cherry fruits were also identified using GC-MS where the main components included 5-Hydroxymethylfurfural (51.18 %) and 4H-Pyran-4-one, 2,3-dihydro-3,5-dihydroxy-6-methyl (21.86%). Our results are indicative of a promising natural product that can be regarded as a new source for insect pest control.  

کلیدواژه‌ها [English]

  • Extract
  • Growth and development
  • Helicoverpa armigera
  • Toxicity
  • Whithania somnifera

© 2024 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

Adams, R. P. (2007) Identification of essential oil components by gas chromatography/mass spectrometry. (Vol. 456, pp. 544-545). Carol Stream: Allured publishing corporation.
Adwas, A. A., Elsayed, A., Azab, A. E. & Quwaydir, F. A. (2019) Oxidative stress and antioxidant mechanisms in human body. Journal of Applied Biotechnology and Bioengineering 6(1), 43-47. https://doi.org/10.15406/jabb.2019.06.00173.
Afraze, Z. & Sendi, J. J. (2021) Immunological and oxidative responses of the lesser mulberry pyralid, Glyphodes pyloalis by an aqueous extract of Artemisia annua L. Invertebrate Survival Journal 75-85. https://doi.org/10.25431/1824-307X/isj.v18i1.75-85.
Afraze, Z., Sendi, J. J., Karimi-Malati, A. & Zibaee, A. (2020) Methanolic extract of winter cherry causes morpho-histological and immunological ailments in mulberry pyralid Glyphodes pyloalis. Frontiers in Physiology 11, 1-16. https://doi.org/10.3389/fphys.2020.00908.
Akanksha, S. R., Islam, A., Arora, R., Singh, H. & Sharma, A. (2022) Update on the preclinical and clinical assessment of Withania somnifera: from ancient Rasayana to modern perspectives. Traditional Medicine Research 7(5), p.46. https://doi.org/10.53388/TMR20220313001.
AlJabr, A. M., Hussain, A., Rizwan-ul-Haq, M. & Al-Ayedh, H. (2017) Toxicity of plant secondary metabolites modulating detoxification genes expression for natural red palm weevil pesticide development. Molecules 22(1), p.169. https://doi.org/10.3390/molecules22010169.
Aqeel, U., Parwez, R., Aftab, T., Khan, M. M. A. & Naeem, M. (2022) Exogenous calcium repairs damage caused by nickel toxicity in fenugreek (Trigonella foenum-graecum L.) by strengthening its antioxidant defense system and other functional attributes. South African Journal of Botany 150, 153-160. https://doi.org/10.1016/j.sajb.2022.07.025.
Basiouny, A. (2021) Enzymatic efficacy of Nimbecidine®, a neem extract, against the phosphatases in certain tissues of the desert locust Schistocerca gregaria (Forskal) (Orthoptera: Acrididae). Archives of Agriculture Sciences Journal 4(1), 127-147. https://dx.doi.org/10.21608/aasj.2021.62324.1054.
Bhatia, A., Bharti, S. K., Tewari, S. K., Sidhu, O. P. & Roy, R. (2013) Metabolic profiling for studying chemotype variations in Withania somnifera (L.) Dunal fruits using GC–MS and NMR spectroscopy. Phytochemistry 93, 105-115. https://doi.org/10.1016/j.phytochem.2013.03.013.
Bian, H. X., Chen, D. B., Li, Y. P., Tan, E. G., Su, X., Huang, J. C., Su, J. F. & Liu, Y. Q. (2022) Transcriptomic analysis of Bombyx mori corpora allata with comparison to prothoracic glands in the final instar larvae. Gene 813, p.146095. https://doi.org/10.1016/j.gene.2021.146095.
Chaitra, S., Prashanth, J. & Jagadeeshkumar, T. S. (2020) Empirical analysis of uric acid in Malpighian tubules and dry excrements and economic traits of the silkworm hybrids. Journal of Entomology and Zoology Studies 8(4), 929-935. https://doi.org/10.22271/j.ento.2020.v8.i4o.7237.
Chapman, R. F. (2013) The insects: structure and function, New York: Cambridge University Press, pp 775.
Chowański, S., Adamski, Z., Marciniak, P., Rosiński, G., Büyükgüzel, E., Büyükgüzel, K., Falabella, P., Scrano, L., Ventrella, E., Lelario, F. & Bufo, S. A. (2016) A review of bioinsecticidal activity of Solanaceae alkaloids. Toxins 8(3), p.60. https://doi.org/10.3390/toxins8030060.
Dar, N. J., Hamid, A. & Ahmad, M. (2015) Pharmacologic overview of Withania somnifera, the Indian ginseng. Cellular and Molecular Life Sciences 72(23), 4445-4460. https://doi:10.1007/s00018-015-2012-1.
Del Poeta, M., Schell, W. A., Dykstra, C. C., Jones, S. K., Tidwell, R. R., Kumar, A., Boykin, D. W. & Perfect, J. R. (1998) In vitro antifungal activities of a series of dication-substituted carbazoles, furans, and benzimidazoles. Antimicrobial agents and chemotherapy 42(10), 2503-2510. https://doi.org/10.1128/aac.42.10.2503.
Dhir, B. (2017) Biofertilizers and biopesticides: eco-friendly biological agents. In Advances in environmental biotechnology. (pp. 167-188). Springer, Singapore. https://doi.org/10.1007/978-981-10-4041-2_10.
Dinesh-Kumar, A., Srimaan, E., Chellappandian, M., Vasantha-Srinivasan, P., Karthi, S., Thanigaivel, A., Ponsankar, A., Chanthini, K. M. P., Shyam-Sundar, N., Annamalai, M. & Kalaivani, K. (2018) Target and non-target response of Swietenia Mahagoni Jacq. chemical constituents against tobacco cutworm Spodoptera litura Fab. and earthworm, Eudrilus eugeniae Kinb. Chemosphere 199, 35-43. https://doi.org/10.1016/j.chemosphere.2018.01.130.
Ellman, G. L., Courtney, K. D., Andres Jr, V. & Featherstone, R. M. (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochemical Pharmacology 7(2), 88-95. https://doi.org/10.1016/0006-2952(61)90145-9.
Fan, Q., Liu, J., Li, Y. & Zhang, Y. (2022) Glutathione S-Transferase May Contribute to the Detoxification of (S)-(−)-Palasonin in Plutella xylostella (L.) via Direct Metabolism. Insects 13(11), p.989. https://doi.org/10.3390/insects13110989.
Gao, X. R., Cui, Y. L., Xu, F. H. & Li, R. F. (1995) The effects SOD scavenging O2−· as CAT existing. Journal of Heibei Normal University (Natural Science) 4, 59-62.
Gao, Y. P., Luo, M., Wang, X. Y., He, X. Z., Lu, W. & Zheng, X. L. (2022) Pathogenicity of Beauveria bassiana PfBb and Immune Responses of a Non-Target Host, Spodoptera frugiperda (Lepidoptera: Noctuidae). Insects 13(10), p.914. https://doi.org/10.3390/insects13100914.
Gaur, R. & Kumar, K. (2010) Insect growth-regulating effects of Withania somnifera in a polyphagous pest, Spodoptera litura. Phytoparasitica 38, 237-241. https://doi.org/10.1007/s12600-010-0092-x.
Gaur, S. K. & Kumar, K. (2017) Bioefficacy of root extracts of a medicinal plant, Withania somnifera (Dunal) against a polyphagous pest, Spodoptera litura (Fabricius) (Lepidoptera: Noctuidae). Archives of Phytopathology and Plant Protection 50 (15-16), 802-814. https://doi.org/10.1080/03235408.2017.1386754.
Gaur, S. K. & Kumar, K. (2019) A comparative bioefficacy of seed and root extracts of a medicinal plant, Withania somnifera when administered to prepupae of lepidopteran insects, Spodoptera litura (Lepidoptera: Noctuidae) and Pericallia ricini (Lepidoptera: Arctiidae). The Journal of Basic and Applied Zoology 80(1), 1-15. https://doi.org/10.1186/s41936-019-0107-1.
Gaur, S. K. & Kumar, K. (2020) Sensitivity of tobacco caterpillar, Spodoptera litura, to extract from a medicinal plant, Withania somnifera. International Journal of Vegetable Science 26(1), 62-78. https://doi.org/10.1080/19315260.2019.1605556.
Gaur, S. K. & Kumar, K. (2020) Toxicity and insect growth regulatory effects of root extract from the medicinal plant, Withania somnifera (Linnaeus) against red flour beetle, Tribolium castaneum (Coleoptera: Tenebrionidae). Archives of Phytopathology and Plant Protection 53(17-18), 856-875. https://doi.org/10.1080/03235408.2020.1802566.
Gaur, S. K. & Kumar, K. (2020) Toxicity and insect growth regulatory activities of medicinal plant, Withania somnifera, in flesh fly, Sarcophaga ruficornis (Diptera: Sarcophagidae). The Journal of Basic and Applied Zoology 81(1), 1-14. https://doi.org/10.1186/s41936-020-00154-2.
Gaur, S. K. & Kumar, K. (2021) Effect of the medicinal plant Withania somnifera on the development of a medico-veterinary pest Chrysomya megacephala (Diptera: Calliphoridae). Invertebrate Reproduction & Development 65(3), 171-187. https://doi.org/10.1080/07924259.2021.1929519.
Go, M., Shin, E., Jang, S. Y., Nam, M., Hwang, G. S. & Lee, S. Y. (2022) BCAT1 promotes osteoclast maturation by regulating branched-chain amino acid metabolism. Experimental & Molecular Medicine 54(6), 825-833. https://doi.org/10.1038/s12276-022-00775-3.
Goharrostami, M., Sendi, J. J., Hosseini, R. & Mahmoodi, N. O. A. (2022) Effect of thyme essential oil and its two components on toxicity and some physiological parameters in mulberry pyralid Glyphodes pyloalis Walker. Pesticide Biochemistry and Physiology 188, p.105220. https://doi.org/10.1016/j.pestbp.2022.105220.
Gonçalves, R. M., Mastrangelo, T., Rodrigues, J. C. V., Paulo, D. F., Omoto, C., Corrêa, A. S. & de AzeredoEspin, A. M. L. (2019) Invasion origin, rapid population expansion, and the lack of genetic structure of cotton bollworm (Helicoverpa armigera) in the Americas. Ecology and Evolution 9(13), 7378-7401. https://doi.org/10.1002/ece3.5123.
Granchi, C., Fortunato, S., Meini, S., Rizzolio, F., Caligiuri, I., Tuccinardi, T., Lee, H. Y., Hergenrother, P. J. & Minutolo, F. (2017) Characterization of the saffron derivative crocetin as an inhibitor of human lactate dehydrogenase 5 in the antiglycolytic approach against cancer. Journal of Agricultural and Food Chemistry 65(28), 5639-5649. https://doi.org/10.1021/acs.jafc.7b01668.
Hasheminia, S. M., Sendi, J. J., Jahromi, K. T. & Moharramipour, S. (2011) The effects of Artemisia annua L. and Achillea millefolium L. crude leaf extracts on the toxicity, development, feeding efficiency and chemical activities of small cabbage Pieris rapae L. (Lepidoptera: Pieridae). Pesticide Biochemistry and Physiology 99(3), 244-249. https://doi.org/10.1016/j.pestbp.2010.12.009.
Isman, M. B. (2023) Commercialization and regulation of botanical biopesticides: a global perspective. In Development and Commercialization of Biopesticides (pp. 25-36). Academic Press. 471 pp.
Javed, M., Majeed, M. Z., Arshad, M., Ahmad, M. H. & Ghafoor, H. A. (2016) Insecticidal potentiality of Eruca sativa (mill.), Piper nigrum (l.) and Withania somnifera (l.) extracts against Trogoderma granarium (everts) (Coleoptera: Dermestidae). International Journal of Fauna and Biological Studies 3(1), 18-20.
Jena, K., Kar, P. K., Kausar, Z. & Babu, C. S. (2013) Effects of temperature on modulation of oxidative stress and antioxidant defenses in testes of tropical tasar silkworm Antheraea mylitta. Journal of Thermal Biology 38(4), 199-204. https://doi.org/10.1016/j.jtherbio.2013.02.008.
John, J. (2014) Therapeutic potential of Withania somnifera: A report on phyto-pharmacological properties. International Journal of Pharmaceutical Sciences Review and Research 5(6), 2131-2148.
Johnson, F. & Giulivi, C. (2005) Superoxide dismutases and their impact upon human health. Molecular Aspects of Medicine 26(4-5), 340-352. https://doi.org/10.1016/j.mam.2005.07.006.
Jun, Z., Dunlun, S. & Jianxin, C. (2003) Physiological and biochemical changes of the silkworm, Bombyx mori infected by Cordyceps militaris. Kun Chong xue bao. Acta Entomologica Sinica 46(6), 674-678.
Kalaivani, T., Rajasekaran, C., Suthindhiran, K. & Mathew, L. (2011) Free radical scavenging, cytotoxic and hemolytic activities from leaves of Acacia nilotica (L.) Wild. ex. Delile subsp. indica (Benth.) Brenan. Evidence-Based Complementary and Alternative Medicine. https://doi.org/10.1093/ecam/neq060.
Kalender, S., Ogutcu, A., Uzunhisarcikli, M., Açikgoz, F., Durak, D., Ulusoy, Y. & Kalender, Y. (2005) Diazinon-induced hepatotoxicity and protective effect of vitamin E on some biochemical indices and ultrastructural changes. Toxicology 211(3), 197-206. https://doi.org/10.1016/j.tox.2005.03.007.
Kaur, K., Dolker, D., Behera, S. & Pati, P. K. (2021) Critical factors influencing in vitro propagation and modulation of important secondary metabolites in Withania somnifera (L.) dunal. Plant Cell, Tissue and Organ Culture pp.1-20. https://doi.org/10.1016/j.indcrop.2021.113872.
Khanchandani, N., Shah, P., Kalwani, T., Ardeshna, A. & Dharajiya, D. (2019) Antibacterial and antifungal activity of Ashwagandha (Withania somnifera l.): A review. Journal of Drug Delivery and Therapeutics 9(5-s), 154-161. https://doi.org/10.22270/jddt.v9i5-s.3573.
Khare, R. K., Das, G., Kumar, S., Bendigeri, S., Sachan, S., Saiyam, R., Banerjee, D. K. & Khare, D. S. (2019) Herbal insecticides and acaricides: Challenges and constraints. International Journal of Chemical Studies 7(4), 118-125.
Khosravi, R. & Sendi, J.J. (2013) Effect of neem pesticide (Achook) on midgut enzymatic activities and selected biochemical compounds in the hemolymph of lesser mulberry pyralid, Glyphodes pyloalis Walker (Lepidoptera: Pyralidae). Journal of Plant Protection Research 53(3), 238-247.
King, J. (1965) The dehydrogenases or oxidoreductases. In: Van Nostrand, D. (Ed.), Lactate Dehydrogenase, Practical Clinical Enzymology, pp. 83-93. London.
Kısa, A., Akyüz, M., Çoğun, H. Y., Kordali, Ş., Bozhüyük, A. U., Tezel, B., Şiltelioğlu, U., Anıl, B. & Çakır, A. (2018) Effects of Olea europaea L. leaf metabolites on the tilapia (Oreochromis niloticus) and three stored pests, Sitophilus granarius, Tribolium confusum and Acanthoscelides obtectus. Records of Natural Products 12(3), p.201. http://doi.org/10.25135/rnp.23.17.07.126.
Krishnan, N. & Kodrík, D. (2006) Antioxidant enzymes in Spodoptera littoralis (Boisduval): are they enhanced to protect gut tissues during oxidative stress?. Journal of Insect Physiology 52(1), 11-20. https://doi.org/10.1016/j.jinsphys.2005.08.009.
Lapcharoen, P., Apiwathnasorn, C., Komalamisra, N., Dekumyoy, P., Palakul, K. & Rongsriyam, Y. (2005) Three indigenous Thai medicinal plants for control of Aedes aegypti and Culex quinquefasciatus. The Southeast Asian Journal of Tropical Medicine and Public Health 36, p.167.
Li, M., Gurram, B., Lei, S., Blum, N. T., Huang, P. & Lin, J. (2021) Recent advances in fluorescence imaging of alkaline phosphatase. Chinese Chemical Letters 32(4), 1316-1330. https://doi.org/10.1016/j.cclet.2020.09.004.
Lowry, O. H. (1951) Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry 193, 265-275.
Luck, H. (1974) Estimation of catalase, methods in enzymatic analysis.
Mageed, A. A., El-bokl, M., Khidr, A. A. & Said, R. (2018) Disruptive effects of selected chitin synthesis inhibitors on cotton leaf worm Spodoptera littoralis (Boisd.). Australian Journal of Basic and Applied Sciences 12(1), 4-9. https://ssrn.com/abstract=3144150.
Marklund, S. & Marklund, G. (1974) Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. European Journal of Biochemistry 47(3), 469-474. https://doi.org/10.1111/j.1432-1033.1974.tb03714.x.
McCord, J. M. & Fridovich, I. (1969) Superoxide dismutase, an enzymatic function for erythrocuprein (hemocurprein). Journal of Biological Chemistry 244(22), 6049-6055.
Mingotti Dias, P., de Souza Loureiro, E., Amorim Pessoa, L. G., Mendes de Oliveira Neto, F., de Souza Tosta, R. A. & Teodoro, P. E. (2019) Interactions between fungal-infected Helicoverpa armigera and the predator Chrysoperla externa. Insects 7, 10-20. https://doi.org/10.3390/insects10100309.
Mojarab-Mahboubkar, M. & Jalali Sendi, J. (2016) Chemical composition, insecticidal and physiological effect of methanol extract of sweet wormwood (Artemisia annua L.) on Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). Toxin Reviews 35(3-4), 106-115. https://doi.org/10.1080/15569543.2016.1203336.
Mojarab-Mahboubkar, M., Sendi, J. J. & Mahmoodi, N. (2022) The sweet wormwood essential oil and its two major constituents are promising for a safe control measure against fall webworm. Pesticide Biochemistry and Physiology 184, p.105124. https://doi.org/10.1016/j.pestbp.2022.105124.
Mojeni, T. D. (2019) Investigating the effect of karvin (53% SC) insecticide on cotton bollworm Helicoverpa armigera (Hub.) in the cotton fields of Golestan province. Applied Sciences 8(6), 119-121.
Murfadunnisa, S., Vasantha-Srinivasan, P., Ganesan, R., Senthil-Nathan, S., Kim, T. J., Ponsankar, A., Kumar, S. D., Chandramohan, D. & Krutmuang, P. (2019) Larvicidal and enzyme inhibition of essential oil from Spheranthus amaranthroids (Burm.) against lepidopteran pest Spodoptera litura (Fab.) and their impact on non-target earthworms. Biocatalysis and Agricultural Biotechnology 21, p.101324. https://doi.org/10.1016/j.bcab.2019.101324.
Nathan, S. S. (2006) Effects of Melia azedarach on nutritional physiology and enzyme activities of the rice leaffolder Cnaphalocrocis medinalis (Guenée) (Lepidoptera: Pyralidae). Pesticide Biochemistry and Physiology 84(2), 98-108. https://doi.org/10.1016/j.pestbp.2005.05.006.
Nation, J. L. (2022) Insect physiology and biochemistry. 4th Edition. CRC press. 586 pp. ISBN: 9781032247045.
Nicolopoulou-Stamati, P., Maipas, S., Kotampasi, C., Stamatis, P., Hens, L. (2016) Chemical pesticides and human health: the urgent need for a new concept in agriculture. Frontiers in Public Health 4, p.148. https://doi.org/10.3389/fpubh.2016.00148.
Oppenoorth, F. J., Van der Pas, L. J. T. & Houx, N. W. H. (1979) Glutathione S-transferase and hydrolytic activity in a tetrachlorvinphos-resistant strain of housefly and their influence on resistance. Pesticide Biochemistry and Physiology 11(1-3), 176-188. https://doi.org/10.1016/0048-3575(79)90057-9.
Otto, A., Oliver, H. & Jane, M. (1946) A method for the rapid determination of alkaline phosphatase with five cubic millimeters of serum. Journal of Biological Chemistry 164(3), 321-329. https://doi.org/10.1016/S0021-9258(18)43072-4.
Pachla, L. A., Reynolds, D. L., Wright, D. S. & Kissinger, P. T. (1987) Analytical methods for measuring uric acid in biological samples and food products. Journal of the Association of the Official Analytical Chemists 70(1), 1-14. https://doi.org/10.1093/jaoac/70.1.1.
Rachokarn, S., Piyasaengthong, N. & Bullangpoti, V. (2008) Impact of botanical extracts derived from leaf extracts Melia azedarach L. (Meliaceae) and Amaranthus viridis L. (Amaranthaceae) on populations of Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae) and detoxification enzyme activities Communications in agricultural and applied biological sciences 73(3), 451-457.
Rahimi, V., Hajizadeh, J., Zibaee, A. & Sendi, J. J. (2018) Effect of Polygonum persicaria (Polygonales: Polygonaceae) extracted agglutinin on life table and antioxidant responses in Helicoverpa armigera (Lepidoptera: Noctuidae) larvae. Journal of Economic Entomology 111(2), 662-671. https://doi.org/10.1093/jee/toy006.
Rai, M., Jogee, P. S., Agarkar, G. & Santos, C. A. D. (2016) Anticancer activities of Withania somnifera: Current research, formulations, and future perspectives. Pharmaceutical Biology 54(2), 189-197. https://doi.org/10.3109/13880209.2015.1027778.
Reddy, K. P., Subhani, S. M., Khan, P. A. & Kumar, K. B. (1985) Effect of light and benzyladenine on dark-treated growing rice (Oryza sativa) leaves II. Changes in peroxidase activity. Plant and Cell Physiology 26(6), 987-994. https://doi.org/10.1093/oxfordjournals.pcp.a077018.
Riaz, S., Johnson, J. B., Ahmad, M., Fitt, G. P. & Naiker, M. (2021) A review on biological interactions and management of the cotton bollworm, Helicoverpa armigera (Lepidoptera: Noctuidae). Journal of Applied Entomology 145(6), 467-498. https://doi.org/10.1111/jen.12880.
Rivera-Pérez, C., Clifton, M. E. & Noriega, F. G. (2017) How micronutrients influence the physiology of mosquitoes. Current Opinion in Insect Science 23, 112-117. https://doi.org/10.1016/j.cois.2017.07.002.
Rizwan-ul-Haq, M., Hu, M. Y., Afzal, M., Bashir, M. H., Gong, L. & Luo, J. (2010) Impact of two medicinal plant extracts on glutathione S-transferase activity in the body tissues of Spodoptera exigua (Lepidoptera: Noctuidae). Pakistan Journal of Botany 42(6), 3971-3979.
Robertson, J. L., Jones, M. M., Olguin, E. & Alberts, B. (2017) Bioassays with arthropods. CRC press.
Saha, I. & Joy, V. C. (2014) Potential ill effects of IGR pesticides on life-history parameters in ecologically important soil collembola Cyphoderus javanus Borner. International Journal of Environmental Science and Technology 3, 365-373. https://doi.org/10.1007/s10661-015-5083-4.
Saheir, F. (2018) Effects of Ocimum sanctum extract against biochemical aspects of Spodoptera littoralis (Lepidoptera: Noctuidae) larvae. Egyptian Journal of Plant Protection Research Institute 1(2), 112-121.
Samada, L. H. & Tambunan, U. S. F. (2020) Biopesticides as promising alternatives to chemical pesticides: A review of their current and future status. Online Journal of Biological Sciences 20, 66-76. https://doi.org/10.3844/ojbsci.2020.66.76.
Shahid, M. R., Farooq, M., Shakeel, M., Ashraf, M., Zia, Z. U., Ahmad, S. & Mahmood, A. (2021) Need for growing non-Bt cotton refugia to overcome Bt resistance problem in targeted larvae of the cotton bollworms, Helicoverpa armigera and Pectinophora gossypiella. Egyptian Journal of Biological Pest Control 31(1), 1-8. https://doi.org/10.1186/s41938-021-00384-8.
Shahriari, M., Sahbzadeh, N., Zibaee, A., Khani, A. & Senthil-Nathan, S. (2017) Metabolic response of Ephestia kuehniella Zeller (Lepidoptera: Pyralidae) to essential oil of Ajwain and thymol. Toxin Reviews 36(3), 204-209. https://doi.org/10.1080/15569543.2017.1294605.
Shanmugaratnam, S., Mikunthan, G. & Thurairatnam, S. (2013) Potential of Withania somnifera Dunal cultivation as a medicinal crop in Jaffna district. American-Eurasian Journal Agriculture and Environment Science 13(3), 357-361. https://doi.org/10.5829/idosi.aejaes.2013.13.03.1941.
Shekari, M., Sendi, J. J., Etebari, K., Zibaee, A. & Shadparvar, A. (2008) Effects of Artemisia annua L. (Asteracea) on nutritional physiology and enzyme activities of elm leaf beetle, Xanthogaleruca luteola Mull. (Coleoptera: Chrysomellidae). Pesticide Biochemistry and Physiology 91(1), 66-74. https://doi.org/10.1016/j.pestbp.2008.01.003.
Shinde, P. K., Vikhe, D. N., Jadhav, R. S. & Shinde, G. S. (2021) Review on Herbal Remedies for Covid-19 (Corona Virus). Research Journal of Science and Technology 13(4), 269-274. https://doi.org/10.52711/2349-2988.2021.00043.
Shorey, H. H. & Hale, R. L. (1965) Mass-rearing of the larvae of nine noctuid species on a simple artificial medium. Journal of Economic Entomology 58(3), 522-524. https://doi.org/10.1093/jee/58.3.522.
Shu, B., Zhang, J., Cui, G., Sun, R., Yi, X. & Zhong, G. (2018) Azadirachtin affects the growth of Spodoptera litura Fabricius by inducing apoptosis in larval midgut. Frontiers in Physiology 9, 137-144. https://doi.org/10.3389/fphys.2018.00137.
Silva, C. T. S., Wanderley-Teixeira, V., Cunha, F. M., Oliveira, J. V., Dutra, K. A., Navarro, D. F. & Teixeira, A. A. C. (2018a) Effects of citronella oil (Cymbopogon winterianus Jowitt ex Bor) on Spodoptera frugiperda (JE Smith) midgut and fat body. Biotechnic and Histochemistry 93(1), 36-48. https://doi.org/10.1080/10520295.2017.1379612.
Silva, I. F., Baldin, E. L., Specht, A., Sosa-Gómez, D. R., Roque-Specht, V. F., Morando, R. & Paula-Moraes, S. V. (2018b) Biotic potential and life table of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) from three Brazilian regions. Neotropical Entomology 47(3), 344-351. https://doi.org/10.1007/s13744-017-0529-8.
Singh, P. & Sharma, Y. K. (2018) Withania somnifera (Ashwagandha): A wonder herb with multiple medicinal properties. Asian Journal of Pharmacy and Pharmacology 4(2), 123-30. https://doi.org/10.31024/ajpp.2018.4.2.5.
Struik, P. C. & Kuyper, T. W. (2017) Sustainable intensification in agriculture: the richer shade of green, A review. Agronomy for Sustainable Development 37(5),1-15. https://doi.org/10.1007/s13593-017-0445-7.
Subramanian, S. & Shankarganesh, K. (2016) Insect hormones (as pesticides). In Ecofriendly pest management for food security (pp. 613-650). Academic Press. https://doi.org/10.1016/B978-0-12-803265-7.00020-8.
Terra, W. R., Barroso, I. G., Dias, R. O. & Ferreira, C. (2019) Molecular physiology of insect midgut. In Advances in insect physiology (56, 117-163). Academic Press. https://doi.org/10.1016/bs.aiip.2019.01.004.
Tetali, S. D., Acharya, S., Ankari, A. B., Nanakram, V. & Raghavendra, A. S. (2021) Metabolomics of Withania somnifera (L.) Dunal: advances and applications. Journal of Ethnopharmacology 267, p.113469. https://doi.org/10.1016/j.jep.2020.113469.
Thakur, N., Kaur, S., Tomar, P., Thakur, S. & Yadav, A. N. (2020) Microbial biopesticides: current status and advancement for sustainable agriculture and environment. In New and future developments in microbial biotechnology and bioengineering (pp. 243-282). Elsevier. https://doi.org/10.1016/B978-0-12-820526-6.00016-6.
Thomas, L. (1998) Alanine aminotransferase (ALT), Aspartate aminotransferase (AST). Clinical Laboratory Diagnostics. 1st ed. Frankfurt: TH-Books Verlagsgesellschaft, 2, 55-65.
Tian, J., Diao, H., Liang, L., Hao, C., Arthurs, S. & Ma, R. (2015) Pathogenicity of Isaria fumosorosea to Bemisia tabaci, with some observations on the fungal infection process and host immune response. Journal of Invertebrate Pathology 130, 147-153. https://doi.org/10.1016/j.jip.2015.08.003.
Tjallinks, G., Boverio, A., Jager, A. W., Kaya, S. G., Mattevi, A. & Fraaije, M. W. (2023) Efficient Oxidation of 5‐Hydroxymethylfurfural Using a Flavoprotein Oxidase from the Honeybee Apis mellifera. ChemBioChem p.e202300588. https://doi.org/10.1002/cbic.202300588.
Toffa, J., Loko, Y. L. E., Kpindou, O. K. D., Zanzana, K., Adikpeto J., Gbenontin Y., Koudamiloro A. & Adandonon A. (2021) Endophytic colonization of tomato plants by Beauveria bassiana Vuillemin (Ascomycota: Hypocreales) and leaf damage in Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) larvae. Egyptian Journal of Biological Pest Control 31(1), 1-9. https://doi.org/10.1186/s41938-021-00431-4.
Trivedi, A., Nayak, N. & Kumar, J. (2017) Fumigant toxicity study of different essential oils against stored grain pest Callosobruchus chinensis. Journal of Pharmacognosy and Phytochemistry 6(4), 1708-1711.
Tunaz, H. & Uygun, N. (2004) Insect growth regulators for insect pest control. Turkish Journal of Agriculture and Forestry 28(6), 377-387.
Vujanović, M., Zengin, G., Đurović, S., Mašković, P., Cvetanović, A. & Radojković, M. (2019) Biological activity of extracts of traditional wild medicinal plants from the Balkan Peninsula. South African Journal of Botany 120, 213-218. https://doi.org/10.1016/j.sajb.2018.06.012.
Warthen Jr, J. D., Stokes, J. B., Jacobson, M. & Kozempel, M. F. (1984) Estimation of azadirachtin content in neem extracts and formulations. Journal of Liquid Chromatography and Related Technologies 7(3), 591-598. https://doi.org/10.1080/01483918408073988.
Williams-Boyce, P. K. & Jungreis, A. M. (1980) Changes in fat body urate synthesizing capacity during the larval-pupal transformation of the tobacco hornworm, Manduca sexta. Journal of Insect Physiology 26(12), 783-789. https://doi.org/10.1016/0022-1910(80)90093-1.
Wilson, J. K., Ruiz, L. & Davidowitz, G. (2019) Dietary protein and carbohydrates affect immune function and performance in a specialist herbivore insect (Manduca sexta). Physiological and Biochemical Zoology 92(1), 58-70. https://doi.org/10.1086/701196.
Wu, K., Li, S., Wang, J., Ni, Y., Huang, W., Liu, Q. & Ling, E. (2020) Peptide hormones in the insect midgut. Frontiers in Physiology 11, p.191. https://doi.org/10.3389/fphys.2020.00191.
Yadav, D. P., Kumar, M. & Jamal, M. A. (2018) Larvicidal and Juvenomimetic property of Withania somnifera extracts against larvae of Tribolium confusum Duavl. International journal of research and analytical reviews 6(1), 559-563.
Yasur, J. & Rani, P. U. (2015) Lepidopteran insect susceptibility to silver nanoparticles and measurement of changes in their growth, development and physiology. Chemosphere 124, 92-102. https://doi.org/10.1016/j.chemosphere.2014.11.029.
Zhang, C., Chen, S. B., Wu, C. Y., Zhang, B. Y., Zhang, Y., Teng, B. & Hu, B. J. (2020) Screening of Beauveria bassiana strains with high virulence against armyworm and activities of protective enzymes in the larvae infected by fungi. Journal of Nuclear Agricultural Sciences 34, 2701-2707.
Zhang, S., Lizhen, F. & Yun, J. (2002) Changes of some biochemical estimates in the hemolymph and body wall of Dendrolimus punctatus infected by Metarhizium anisopliae. Kun Chong zhi shi=Kunchong Zhishi 39(4), 297-300.
Zhao, T., Lai, D., Zhou, Y., Xu, H., Zhang, Z., Kuang, S. & Shao, X. (2019) Azadirachtin A inhibits the growth and development of Bactrocera dorsalis larvae by releasing cathepsin in the midgut. Ecotoxicology and Environmental Safety 183, p.109512. https://doi.org/10.1016/j.ecoenv.2019.109512.
Zibaee, A., Zibaee, I. & Sendi, J. J. (2011) A juvenile hormone analog, pyriproxifen, affects some biochemical components in the hemolymph and fat bodies of Eurygaster integriceps Puton (Hemiptera: Scutelleridae). Pesticide Biochemistry and Physiology 100(3), 289-298. https://doi.org/10.1016/j.pestbp.2011.05.002.