مطالعه اثر ترکیب عصاره گیاه کرفس، L. (Apiaceae) Apium graveolens، با باکتریBacillus thuringiensis ، علیه بید سیب‌زمینی، Phthorimaea operculella (Lep.: Gelechiidae)

نوع مقاله : مقاله پژوهشی

نویسندگان

1 گروه گیاه پزشکی، دانشکده کشاورزی، دانشگاه شهید مدنی آذربایجان، تبریز،ایران

2 گروه گیاه پزشکی، دانشکده کشاورزی، دانشگاه تبریز، تبریز، ایران

3 گروه گیاه پزشکی، دانشکده کشاورزی، دانشگاه شهید مدنی آذربایجان، تبریز، ایران

4 گروه گیاه پزشکی، دانشکده کشاورزی، دانشگاه تبریز، تبریز، ایران.

چکیده

بید سیب­زمینی، Phthorimaea operculella، یکی از آفات بسیار مهم سیب­زمینی است که سالانه خسارات اقتصادی زیادی را در انبار و مزرعه وارد می­کند. در این بررسی تأثیر تلفیق حشره­کش میکروبی Bt با عصاره­های هگزانی، اتیل­استاتی و متانولی گیاه کرفس، Apium graveolens، بر مرگ و میر و برخی پارامترهای زیستی این آفت مطالعه شده است. عصاره­گیری با روش خیساندن انجام گرفت. غلظت­های زیرکشنده عوامل مورد بررسی شامل LC50، LC30 و LC10 به­صورت انفرادی و در تلفیق با یکدیگر به­صورت گوارشی مورد بررسی قرار گرفتند. برگ­های هم­سن و هم­اندازه سیب­زمینی در هر کدام از تیمارها غوطه­ور شده و پس از خشک شدن در اختیار لاروهای سن اول بید سیب­زمینی قرار گرفت. اثرات کشندگی هر غلظت و تلفیق دو عامل در فواصل زمانی 48، 96 و 144 ساعت ثبت گردید. همچنین اثر مهارکنندگی عصاره­ها بر آنزیم­های آلفا-آمیلاز و پروتئاز لاروهای بید سیب­زمینی نیز مورد مطالعه قرار گرفت. نتایج نشان داد که عصاره اتیل­استاتی کرفس در تلفیق با باکتری Bt اثرات سینرژیستی بر مرگ و میر لاروها داشت. تلفیق باکتری Bt با عصاره متانولی اثرات کشندگی کمتری نشان داد. همچنین مشخص گردید که تلفیق غلظت­های زیرکشنده عوامل مورد بررسی تأثیر معنی­داری بر طول دوره رشدی لاروی داشته و به­طور معنی­داری آن را افزایش دادند. همچنین درصد ظهور حشرات کامل به­شدت تحت تأثیر قرار گرفته و بخصوص در تلفیق غلظت­های LC50 عصاره­ها و حشره­کش Bt، به شدت کاهش یافت. نتایج مطالعات آنزیمی نشان داد که عصاره اتیل­استاتی کرفس در غلظت 10درصد 77/37 درصد فعالیت آنزیم پروتئاز و 51/25 درصد فعالیت آنزیم آلفا-آمیلاز لاروهای بید سیب­زمینی را مهار کردند.

کلیدواژه‌ها

موضوعات

عنوان مقاله [English]

Studying the Combination Effect of Celery, Apium graveolens Extracts with Bt, Against Potato Tuber Moth Phthorimaea operculella

نویسندگان [English]

  • Davoud Mohammadi 1
  • Akram Hatami 2
  • Naser Eivazian Kary 3
  • Reza Farshbaf Pourabad 4
1 Department of Plant Protection, Faculty of Agriculture, Azarbaijan Shahid Madani University, Tabriz, Iran
2 Department of Plant Protection, Faculty of Agriculture, University of Tabriz, Tabriz, Iran
3 Department of Plant Protection, Faculty of Agriculture, Azarbaijan Shahid Madani University, Tabriz, Iran
4 Department of Plant Protection, Faculty of Agriculture, University of Tabriz, Tabriz, Iran
چکیده [English]

Introduction[1]
Potato tuber moth, Phthorimaea operculella is an important pest of potatoes which annually impose economic loss in potato production especially in stored places. Chemical control with spray in farms and fumigation in storages is a conventional method for depressing the population of this pest. In addition, with harmful effects of synthetic pesticides on environment and human health, developing resistant population of insects, compel researchers and plant protection institutions to utilizing new safe control methods. Delaying the resistance by keeping effectiveness of pesticides by using synergists and sublethal concentrations is a resistance management method. Bacillus thuringiensis is an effective microbial control agent against some insects. Its effectiveness decreased because of developing resistance in some population of insects. Combination of Bt with some botanical biopesticides increases its efficiency that reported in many studies. In this study combination of B. thuringiensis with hexane, ethyl acetate and methanol extracts of Celery, Apium graveolens were investigated on mortality and some biological parameters of PTM. Celery is a biennial plant in the apiaceae family, which is rich in some compounds such as phenolic and flavonoids. These compounds could affect biology and physiology of insects. Combination of sublethal concentrations of Bt with extracts of celery subjected for study of their effects on mortality, synergistic effects and some biological parameters on PTM larvae in this paper.
 
Materials and Methods
Potato tuber moth colony established by preparing larvae from a health colony in department of plant protection, Azarbaijan Shahid Madani university. Larva reared on potato tubers in plastic containers. Rearing carried out in controlled condition of 26±2ºC, 60% RH and a photoperiod of 16:8 (L: D) hrs.
Foliage of celery after well washing with distilled water, dried in shadow in laboratory condition. Coarsely powdered dry plants used for extraction. Extraction carried out using the maceration method with three solvents, hexane, ethyl acetate and methanol respectively. Sub-lethal concentrations of both agents, including LC10, LC30 and LC50, individually and in combination, were assayed by the oral bioassay method. The same age and size of potato leaves were impregnated with sub-lethal concentrations of both experimental materials using the dipping method. The first larval instars of PTM were transferred on treated leaves, and mortality was recorded in 48, 96 and 144 hours’ intervals. Larval developmental period and adult’s emergence as an important biological parameter recorded in all treatments. In addition, the inhibitory activity of extracts on α-amylase and protease enzyme of PTM larva was considered.
Inhibitory activity of celery extracts in two concentrations 1 and 10%, on PTM larvae alpha-amylase activity was assayed by the dinitrosalicylic acid procedure, using 1% soluble starch as a substrate described by Bernfeld, (1955). And protease inhibitory activity assayed using azocasein as substrate, with comparing enzyme activity in controls and present of extracts in reactions.
All experiments were replicated three times. On-way ANOVA analysis of variance in random design was used for statistical analysis. Duncan’s multiple range tests used for comparing means. For determining the synergistic, additive or antagonistic effects of combinations, chi-square test conducted between observed and expected results (df=1).
 
Results and Discussion
The results revealed that ethyl acetate extract of celery in combination with Bt synergistically increased the mortality of larvae. Compared to the control, the combination of methanolic extract with Bt didn’t affect larval mortality. However, the combination of sub-lethal concentrations significantly increased larval life span compared with the control and adult emergence decreased especially in LC50 combinations. Increasing the mortality with exposure time progressing, observed in all combinations and the most larval mortality recorded in 144 hours’ exposure time. Ethylacetate extract of celery alone and in combination with Bt more than other solvents affected biological parameters of PTM. Extracts in the concentration of 10 percent in reactions inhibited α-amylase and protease activity of PTM larvae by 27.97-37.77 and 11.48-25.51 percent, respectively.
Numerous researchers have reported increased efficiency of Bt in combination with other plant extracts for controlling various insects. The observed synergistic effects can be attributed to factors such as disrupting midgut properties, inhibiting digestive enzyme activity, and disrupting the insect's immune system by plant extracts.Inhibitory activity of celery extracts on digestive enzymes activity of PTM larva, well documented in this research which is in alignment with other reports. Effects on larval life span that with prolonging it affects population dynamics of insect pests, reported in same studies. This biological effect has adverse effect on development and physiology of insects and asynchronies developmental stage with environmental variations which finally decrease the population of next generations or overwintering insect’s density. Adults and pupa emergence percentage decreased in combination of Bt with celery extracts that same results were reported in other researches.
 
Conclusion
This study aims to determine the effects of different extracts (prepared by different solvents) of celery in combination with Bt on potato tuber moth larvae. Effects of different solvents in separating effective compounds on PTM, was not same. In certain instances, the methanol extract of celery showed a minor effect in enhancing the potency of Bt. However, strong synergistic effects were observed with ethyl acetate and hexane extracts at various integrated concentrations. Time also played a crucial role in achieving the desired mortality results, with mortality and synergistic effects increasing over time in all extract combinations with Bt. Particularly, towards the end of the exposure period, a synergistic effect was notably observed in all integrations involving ethyl acetate extract of celery.In addition, with mortality, larval developmental period also affected by combinations. Increasing in life span observed in all treatments with different ratios. Adult emergence decreased strongly in different treatments and this is so important in decreasing the population of PTM. Because of importance of Bt as an effective and safe insecticide and increasing the resistance by different pests such as PTM, management of insects in integrated programs using plant extracts will improve the efficiency of Bt. Decreasing the sprayed concentrations in combination with other control methods are two important resistance management toll in IPM programs. Celery is a potent plant for this goal and additional studies are needed.    
 



 
 



 
 

کلیدواژه‌ها [English]

  • Biological effects
  • Enzyme inhibition
  • Larval life span
  • Sublethal concentrations
  • Synergistic effects

©2023 The author(s). This is an open access article distributed under Creative Commons Attribution 4.0 International License (CC BY 4.0), which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source.

  

مراجع

  1. Abedi, Z., Saber, M., Vojoudi, S., Mahdavi, V., & Parsaeyan, E. (2014). Acute, sublethal, and combination effects of azadirachtin and Bacillus thuringiensis on the cotton bollworm, Helicoverpa armigera. Journal of Insect Science, 14, 30. https://doi.org/10.1093/jis/14.1.30
  2. Aghaali, N., Ghadamyari, M., Hosseininaveh, V., & Saberi Riseh, N. (2013). Protease inhibitor from the crude extract of plant seeds affects the digestive proteases in Hyphantria cunea (Lep.: Arctiidae). Journal of Plant Protection Research, 53(4), 338-346. https://doi.org/10.2478/jppr-2013-0051
  3. Ali, K., Sagheer, M., ul Hasan, M., Rashid, A. & Shahid, M. (2021). Bioactivity of medicinal plant extracts as toxicants and enzyme inhibitors against insect pests of stored commodities. Journal of Crop Protection, 10(1), 95-109. https://doi.org/20.1001.1.22519041.2021.10.1.11.5
  4. Allahverdizadeh, N.M., & Mohammadi, D. (2016). Bioactivity of Marrubium vulgare and Achillea millefolium leaf extracts on potato tuber moth Phthorimaea operculella Munis Entomology and Zoology, 11(1), 114-122.
  5. Alvarez, J.M., Dotseth, E., & Nolte, P. (2005). Potato tuber worm: a threat for Idaho potatoes. University of Idaho Experiment Station Bulletine, CIS1125 1-4.
  6. Alves, T.J.S., Cruz, G.S., Wanderley‐Teixeira, V., Teixeira, A.A.C., Oliveira, J.V., Correia, A.A., Câmara, A.A.G., & Cunha, F.M. (2013). Effects of Piper hispidinervum on spermatogenesis and histochemistry of ovarioles of Spodoptera frugiperda. Biotechnic and Histochemistry, 88, 1–11. https://doi.org/13109/10520295.2013.837509
  7. Bernfeld, P. (1955) Amylase α and β. Methods in Enzymology, 1, 149-158. https://doi.org/10.1016/0076-6879(55)01021-5
  8. Candido, L.P., Cavalcanti, M.T., & Beserra, E.B. (2013). Bioactivity of plant extracts on the larval and pupal stages of Aedes aegypti (Diptera, Culicidea). Revista da Sociedade Brasileira de Medicina Tropical, 46(4), 420-425. https://org/10.1590/0037-8682-0118-2013
  9. Capinera, J.L. (2020). Handbook of vegetable pests. Academic Press, New York.
  10. Da Lage, J-L. (2018). The amylases of insects. International Journal of Insect Science, 10, 1–14. https://org/10.1177/1179543318804783
  11. de França, S.M., Breda, M.O., Barbosa, D.R.S., Araujo, A.M.N., & Guedes, C.A. (2017). The sublethal effects of insecticides in insects. In: Shields, V.D.C. (Ed.), Biological Control of Pest and Vector Insects, Intech Open. https://doi.org/10.5772/66461
  12. Dekebo, A., Aryal, S., & Jung, C. (2019). Olfactory responses of adult potato tuber moth, Phthorimaea operculella (Zeller) measured by attraction relative to the tomato leaf volatiles. Journal of Asia-Pacific Entomology, 22, 611–618. https://org/10.1016/j.aspen.2019.04.007
  13. Dirar, A.I., Alsaadi, D.H.M., Wada, M., Mohamed, M.A., Watanabe, T., & Devkota, H.P. (2019). Effects of extraction solvents on total phenolic and flavonoid contents and biological activities of extracts from Sudanese medicinal plants. South African Journal of Botany, 120, 261-267. https://org/10.3390/agriculture12111820
  14. Dogramaci, M., & Tingey, W. (2008). Comparison of insecticide resistance in a North American field population and a laboratory colony of potato tuber worm (Lepidoptera: Gelechiidae). Journal of Pest Science, 81, 17-22. https://doi.org/10.1007/s10340-007-0178-5
  15. Dolores Ibáñez, M., Sanchez-Ballester, N.M., & Amparo Blázquez, M. (2020). Encapsulated limonene: a pleasant lemon-like aroma with promising application in the agri-food industry. A review. Molecules, 25, 1-20. https://org/10.3390/molecules25112598
  16. El-kady, H. (2011). Insecticide resistance in potato tuber moth Phthorimaea Operculella Zeller in Egypt. Journal of American Science, 7(10), 263-266.
  17. El-Wakeil, N.E. (2013). Botanical pesticides and their mode of action. Gesunde Pflanzen, 65, 125–149. https://org/10.1007/s10343-013-0308-3
  18. Fouad Sharaby, A.M., Gesraha, M.A., & Baker Fallatah, S.A. (2019). Integration of some biopesticides against potato tuber moth, Phthorimaea operculella (Zell.), during storage with reference to histopathological changes detected by a transmission electron microscope in the endocrine system. Bulletin of the National Research Centre, 43, 1-16. https://org/10.1186/s42269-019-0163-1
  19. Gujar, G.T., Kalia, V., Kumari, A., & Prasad, T.V. (2004). Potentiation of insecticidal activity of Bacillus thuringiensis kurstaki HD-1 by proteinase inhibitors in the American bollworm, Helicoverpa armigera (Hübner). Indian Journal of Experimental Biology, 42, 157-163.
  20. Handa, S.S., Singh Khanuja, S.P., Longo, G., & Rakesh, D.D. (2008). Extraction technologies for medicinal and aromatic plants. International center for science and high technology, 260 P.
  21. Hatami, A., Mohammadi, D., & Eivazian Kary, N. (2022). Comparing oral toxicity of Apium graveolens and Falcaria vulgaris extracts with Bt against Phthorimaea operculella (Zeller). Journal of Applied Research in Plant Protection, 11(3), 17-29. (In Persian with English abstract). https://doi.org/10.22034/ARPP.2022.15186
  22. Hussain Shah, T. (2017). Plant nutrients and insect’s development. International Journal of Entomology Research, 2(6), 54-57.
  23. Ibrahim, M.A., Kainulainen, P., Aflatuni, A., Tiilikkata, K., & Holopainen, J.K. (2001). Insecticidal, repellent, antimicrobial activity and phytotoxicity of essential oils: With special reference to limonene and its suitability for control of insect pests. Agricultural and Food Science in Finland, 10, 243-259. https://doi.org/10.23986/afsci.5697
  24. Isman, M.B. (2020). Botanical insecticides in the twenty-first century–fulfilling their promise? Annual Review Entomology, 65, 233–249. https://doi.org/10.1146/annurev-ento-011019-025010
  25. Jung, J-M., Lee, S-G., Kim, K.H., Jeon, S.W., Jung, S., & Lee, W.H. (2019). The potential distribution of the potato tuber moth (Phthorimaea Operculella) based on climate and host availability of potato. Agronomy, 10, 12. https://doi.org/10.3390/agronomy10010012
  26. Karr, L.L., & Coats, J.R. (1988). Insecticidal properties of d-limonene. Journal of Pesticide Science, 13, 2287–2290. https://doi.org/10.1584/jpestics.13.287
  27. Khalil, A., Nawaz, H., Ghania, JB., Rehman, R., & Nadeem, F. (2015). Value added products, chemical constituents and medicinal uses of celery (Apium graveolens) – a review. International Journal of Chemical and Biochemical Sciences, 8, 40-48.
  28. Khan, S., Nazir Uddin, M., Rizwan, M., Khan, W., Farooq, M., Shah, A., Subhan, F., Aziz, F., Ur Rahman, K., Khan, A., Ali, S., & Muhammad, M. (2020). Mechanism of insecticide resistance in insects/pests. Polish Journal of Environmental Studies, 29(3), 2023–2030. https://doi.org/10.15244/pjoes/108513
  29. Khorrami, F., & Soleymanzade, A. (2021). Efficacy of some chemical insecticides and plant extracts combined with Bacillus thuringiensis against Phthorimaea operculella. Acta phytopathologica et entomologica Hungarica, 56(2), 169-179. https://doi.org/10.1556/038.2021.00119
  30. Konecka,, Kaznowski, A., Grzesiek, W., Nowicki, P., Czarniewska, E., & Baranek, J. (2020). Synergistic interaction between carvacrol and Bacillus thuringiensis crystalline proteins against Cydia pomonella and Spodoptera exigua. BioControl, 65, 447–460. https://doi.org/10.1007/s10526-020-10011-4
  31. Kooti, W., Ali-Akbari, S., Asadi-Samani, M., Ghadery, H., & Ashtary-Larky, D. (2014). A review on medicinal plant of Apium graveolens. Advanced Herbal Medicine, 1(1), 48-59.
  32. Koppenhöfer, A.M., & Kaya, H.K. (1997). Synergism of imidacloprid and an entomopathogenic nematode: a novel approach to white grub (Coleoptera: Scarabaeidae) control in turfgrass. Journal of Economic Entomology, 91, 618–623. https://doi.org/10.1093/jee/91.3.618
  33. Koul, O., Walia, S., & Dhliwal, G. (2008). Essential oils as green pesticides: potential and constraints. Biopesticides International, 4(1), 63-84.
  34. Kuppusamy, P., Yusoff, M.M., Maniam, G.P., & Govindan, N., (2016). Biosynthesis of metallic nanoparticles using plant derivatives and their new avenues in pharmacological applications - An updated report. Saudi Pharmaceutical Journal, 24(4), 473-84. https://doi.org/10.1016/j.jsps.2014.11.013
  35. Le, A.V., Parks, S.E., Nguyen, M.H., & Roach, P.D. (2018). Effect of solvents and extraction methods on recovery of bioactive compounds from defatted gac (Momordica cochinchinensis) seeds. Separations, 5, 39. https://doi.org/10.3390/separations5030039
  36. Lee, C.Y. (2000). Sublethal effects of insecticide on longevity, fecundity, and behavior of insect pests: a review. Bioscience Journal, 11, 107–112. https://doi.org/10.5772/66461
  37. Lezoul, N.H., Belkadi, M., Habibi, F., & Guillén, F. (2020). Extraction processes with several solvents on total bioactive compounds in different organs of three medicinal plants. Molecules, 25, 4672. https://doi.org/10.3390/molecules25204672
  38. Madasamy,, Sahayaraj, K., Sayed, S.M., Al-Shuraym, L.A., Selvaraj, P., El-Arnaouty, S.A. & Madasamy, K. (2023). Insecticidal mechanism of botanical crude extracts and their silver nanoliquids on Phenacoccus solenopsis. Toxics, 11, 305. https://doi.org/10.3390/toxics11040305
  39. Magholi Fard, Z., Hesami, S., Marzban, R., & Salehi Jouzani, G. (2020). Individual and combined biological effects of Bacillus thuringiensis and multicapsid Nucleopolyhedrovirus on the biological stages of egyptian cotton leafworm, Spodoptera littoralis (B.) (Lep.: Noctuidae). Journal of Agricultural Science Technology, 22(2), 465-476. https://doi.org/20.1001.1.16807073.2020.22.2.13.1
  40. Malik, K., & Riasat, R. (2014). Study of combined effect of locally isolated Bacillus thuringiensis and turmeric powder on red flour beetle (Tribolium castaneum). International Journal of Current Microbiology Applied Science, 3, 760–77. https://doi.org/10.5829/idosi.aje.2015.8.1.9244
  41. Mehrabadi, M., Bandani, A.R., & Alizadeh, H. (2012). Inhibitory activity of proteinaceous alpha- amylase inhibitors from Triticale seeds against Eurygaster integriceps salivary alpha-amylases: Interaction of the inhibitors and the insect digestive enzymes. Pesticide Biochemistry and Physiology, 102, 220-228. https://doi.org/10.1016/j.pestbp.2012.01.008
  42. Mesén-Porras, E., Dahdouh-Cabia, S., Jimenez-Quiros,c., Mora-Castro, R., Rodríguez, C., & Pinto-Tomás, A. (2020).Soybean protease inhibitors increase Bacillus thuringiensis Israelensis toxicity against Hypothenemus hampei. Agronomía Mesoamericana, 31(2),461-478. https://doi.org/10.15517/am.v31i2.36573
  43. Mohammadi, D., Eivazian Kary, N., & Sharifi Azar, Z. (2020). Enhancing Efficiency of Bacillus thuringiensis by Leaf Extract of Cupressus arizonica against Spodoptera exigua (Lep.: Noctuidae). Journal of Applied Research in Plant Protection, 9(1), 89-105. (In Persian with English abstract)
  44. Nazarpour, L., Yarahmadi, F., Saber, M., & Rajabpour, A. (2016). Short and long term effects of some bio-insecticides on Tuta absoluta Meyrick (Lepidoptera: Gelechiidae) and its coexisting generalist predators in tomato fields. Journal of Crop Protection, 5(3), 331-342. https://doi.org/20.1001.1.22519041.2016.5.3.7.0
  45. Ngegba, P.M., Cui, G., Khalid, M.Z., & Zhong, G. (2022). Use of botanical pesticides in agriculture as an alternative to synthetic pesticides. Agriculture, 12(5), 600. https://doi.org/10.3390/agriculture12050600
  46. Nouri-Ganbalani, G., Borzoui, E., Abdolmaleki, A., Abedi, Z., & George Kamita, S. (2016). Individual and combined effects of Bacillus thuringiensis and Azadirachtin on Plodia interpunctella Hübner (Lepidoptera: Pyralidae). Journal of Insect Science, 16(1), 95. https://doi.org/10.1093/jisesa/iew086. PMID: 27638953
  47. Opender, K., & Walia, S. (2009). Comparing impacts of plant extracts and pure allelochemicals and implications for pest control. Cab Reviews: Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources 4, 1-30. https://doi.org/10.1079/PAVSNNR20094049
  48. Plata-Rueda, A., Quintero, H.A., Serrão, J.E., & Martínez, L.C. (2020). Insecticidal activity of Bacillus thuringiensis strains on the nettle caterpillar, Euprosterna elaeasa (Lepidoptera: Limacodidae). Insects, 11, 310. https://doi.org/10.3390/insects11050310
  49. Qi, X.-J., Feng, Y.X., Pang, X., & Du, S.S. (2021). Insecticidal and repellent activities of essential oils from seed and root of celery (Apium graveolens) against three stored product insects. Journal of Essential Oil Bearing Plants, 24(5), 1169-1179, https://doi.org/10.1080/0972060X.2021.1981159
  50. Rajguru, M., & Sharma, A.N. (2012). Comparative efficacy of plant extracts alone and in combination with Bacillus thuringiensis sub sp. kurstaki against Spodoptera litura larvae. Journal of Biopesticides, 5(1), 81-86.
  51. Rajguru, M., Sharma, A., & Banerjee, S. (2011). Assessment of plant extracts fortified with Bacillus thuringiensis (Bacillales: Bacillaceae) for management of Spodoptera litura (Lepidoptera: Noctuidae). International Journal of Tropical Insect Science, 31(1-2), 92-97. https://doi.org/10.1017/S174275841100018X
  52. Reddy, D.S., & Chowdary, N.M. (2021). Botanical biopesticide combination concept- a viable option for pest management in organic farming. Egyptian Journal of Biological Pest Control, 31, 1-10. https://doi.org/10.1186/s41938-021-00366-w
  53. Rondon, S.I. (2010). The potato tuberworm: a literature review of its biology, ecology, and control. American Journal of Potato Research, 87, 149–166. https://doi.org/10.1007/s12230-009-9123-x
  54. Rożek, E., Nurzyńska-Wierdak, R., Sałata, A., & Gumiela P. (2016). The chemical composition of the essential oil of leaf celery (Apium graveolensl. var. Secalinum Alef.) under the plants’ irrigation and harvesting method. Acta Scientiarum Polonorum Hortorum Cultus, 15(1), 147-157.
  55. Sánchez–Yáñez, J.M., Rico, J.L., & Ulíbarri, G. (2022). Bacillus thuringiensis (Bt) is more than a special agent for biological control of pests. Journal of Applied Biotechnology and Bioengineering, 9(2), 33‒39. https://doi.org/15406/jabb.2022.09.00282
  56. Schoor, T.V., Kelly, E.T., Tam, N., & Michael Attardo, G. (2020). Impacts of dietary nutritional composition on larval development and adult body composition in the yellow fever mosquito (Aedes aegypti). Insects, 11, 535. https://doi.org/10.3390/insects11080535
  57. Senthil-Nathan, S., Kandaswamy, K., Kim, S., & Kadarkarai, M. (2006). The toxicity and behavioural effects of neem limonoids on Cnaphalocrocis medinalis (Guenée) the rice leaf-folder. Chemosphere, 62, 1381-7. https://doi.org/10.1016/j.chemosphere.2005.07.051
  58. Silva, C.T.S., Wanderley‐Teixeira, V., Cunha, F.M., Oliveira, J.V., Dutra, K.A., Navarro, D.M.A.F., & Teixeira, A.A.C. (2016). Biochemical parameters of Spodoptera frugiperda treated with citronella oil (Cymbopogon wintwrianus Jowitt ex Bor) and its influence on reproduction. Acta Histochemistry, 118, 347–352. https://doi.org/10.1016/j.acthis.2016.03.004
  59. Singh Rattan, R. (2010). Mechanism of action of insecticidal secondary metabolites of plant origin. Crop Protection, 29(9), 913-920. https://doi.org/1016/j.cropro.2010.05.008
  60. Stark, J.D., & Banks, J.E. (2003). Population‐level effects of pesticides and other toxicants on arthropods. Annual Review of Entomology, 48, 505–519. https://doi.org/10.1146/annurev.ento.48.091801.112621
  61. Sun, J., Feng, Y., Wang, Y., Li, J., Zou, K., Liu, H., Hu, Y., Xue, Y., Yang, L., Shushan, Du, S., & Wu, Y. (2020). Investigation of pesticidal effects of Peucedanum terebinthinaceum essential oil on three stored-product insects. Records of Natural Products, 14(3), 177-189.
  62. Talaei-Hassanloui, R., Bakhshaei, R., Hosseininaveh, V., & Khorramnezhad, A. (2014). Effect of midgut proteolytic activity on susceptibility of lepidopteran larvae to Bacillus thuringiensis Kurstaki. Frontiers in Physiology, 4, 406. https://doi.org/10.3389/fphys.2013.00406
  63. Theochari, I., Giatropoulos, A., Papadimitriou, V., Karras, V., Balatsos, G., Papachristos, D., & Michaelakis, A. (2020). Physicochemical characteristics of four limonene-based nanoemulsions and their larvicidal properties against two mosquito species, Aedes albopictus and Culex pipiens Insects, 11, 1-12. https://doi.org/10.3390/insects11110740
  64. Vilani, A., Lozano, E.R., Potrich, M., Angeli, A., Luis, F., Martins, C.M.F., Dall Agnol de Lima, J., & de Gouvea, A. (2017). Activity of plant aqueous extracts on Bacillus thuringiensis and their interactions on Anticarsia gemmatalis (Lepidoptera: Erebinae). Semina: Ciências Agrárias, 38(2), 1051-1057. https://doi.org/10.5433/1679-0359.2017v38n2p1051
  65. Visweshwar, R., Akbar, S.M.D., Sharma, H.C., & Sreeramulu, K. (2018). Influence of Bacillus thuringiensis toxins on the development and midgut proteases in different larval instars of Helicoverpa armigera. Indian Journal of Entomology, 80(3), 960-970.
  66. Yang, J., Quan, Y., Sivaprasath, P., Shabbir, M.Z., Wang, Z., Ferré, J., & He, K. (2018). Insecticidal activity and synergistic combinations of ten different Bt toxins against Mythimna separata (Walker). Toxins, (Basel), 4;10(11): 454. https://doi.org/10.3390/toxins10110454
  67. Yazdani, E., JalaliSendia, J., Zibaeea, A., & Ghadamyari, M. (2010). Enzymatic properties of α-amylase in the midgut and the salivary glands of mulberry moth, Glyphodespyloalis Walker (Lepidoptera: Pyralidae). Comptes Rendus Biologies, 333(1), 17-22.
  68. Yildirim, E., Emsen, B., & Kordali, S. (2013). Insecticidal effects of monoterpenes on Sitophilus zeamais Motschulsky (Coleoptera: Curculionidae). Journal of Applied Botany and Food Quality, 86, 198-204.
  69. Zhang, C., Yu, J., Tu, Q., Yan, F., Hu, Z., Zhang, Y., & Song, C. (2022). Antioxidant capacities and enzymatic inhibitory effects of different solvent fractions and major flavones from celery seeds produced in different geographic areas in China. Antioxidants, 11, 1542. https://doi.org/10.3390/antiox11081542
  70. Zhu, F., Lavine, L., O’Neal, S., Lavine, M., Foss, C., & Walsh, D. (2016). Insecticide resistance and management strategies in urban ecosystems. Insects, 7, 2. https://doi.org/10.3390/insects7010002
ارسال نظر در مورد این مقاله
CAPTCHA Image

فایل ها

هم رسانی

ارجاع به این مقاله

آمار