Lethal effects of essential oils from eight Iranian pharmaceutical plants against two stored-product lepidopterans and their chemical composition

Document Type : Research paper-Persian

Authors

1 Assistant Professor, Department of Plant Protection, Faculty of Plant Production, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran

2 M.Sc. Graduated,, Department of Plant Protection, Faculty of Plant Production, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan Iran

Abstract

Background and Objectives

To produce high-quality food and minimize risks from chemical applications, employing economically viable alternative methods without chemical-related drawbacks is vital. Plant essential oils (EOs) have garnered attention as potential insect pest control agents. The current study examines the lethal effects of plant EOs on the Mediterranean flour moth (Ephestia kuehniella Zeller) and the Indian meal moth (Plodia interpunctella (Hübner)).

Materials and Methods

This study examined the fumigant toxicity of eight Iranian pharmaceutical plant EOs: sweet wormwood (Artemisia annua), black cumin (Elwendia persica), Shirazi thyme (Zataria multiflora), costmary (Tanacetum balsamita), galbanum (Ferula gummosa), myrtle (Myrtus communis), lemon (Citrus × limon) and marjoram (Origanum majorana) against eggs, first instar larvae, and adults of P. interpunctella and E. kuehniella. Insects were maintained under controlled conditions at 27 ± 2 °C, 60 ± 5% R.H., and a photoperiod of 14L:10D. Gas Chromatography-Mass Spectrometry (GC-MS) was employed to identify the compounds present in the tested plant EOs. The lethal concentration (LC) values were estimated using probit analysis based on data obtained from preliminary and main bioassays.

Results

The predominant compounds (in term of %) identified in the EOs were as follows: A. annua: Camphor (41.388), 1,8-Cineole (13.431); E. persica: α-Terpinolen (31.622), Limonene (14.524), Propanal, 2-methyl-3-phenyl- (13.180); Z. multiflora: Carvacrol (60.593) and Terbutaline, tris (trimethyl silyl) ether (11.229); T. balsamita: Carvone (42.607), (‒)-Thujanone (17.600); F. gummosa: β-Thujene (34.234), β-pinene (22.371); M. communis: δ-3-Carene (30.549), 1,8-Cineole (19.580), Carvacrol (13.987); C. limon: Limonene (55.131), and O. majorana: (‒)-Terpinen-4-ol (34.138), γ-Terpinene (15.494). EOs exhibited comparable ovicidal activity against the eggs of both species. Notably, A. annua EO displayed the highest efficacy, with LC50 values of 58.12 μl/L air for E. kuehniella and 51.55 μl/L air for P. interpunctella. For E. kuehniella, the EOs of M. communis, Z. multiflora, and F. gummosa followed suit in terms of efficacy, while E. persica, O. majorana, T. balsamita, and C. limon EOs demonstrated the lowest ovicidal activity. Conversely, regarding P. interpunctella, the EOs of M. communis, F. gummosa, Z. multiflora and E. persica exhibited the next highest efficacy, whereas T. balsamita, O. majorana, and C. limon EOs displayed the least ovicidal activity. Eggs of P. interpunctella exhibited slightly greater sensitivity compared to those of E. kuehniella. The EOs of M. communis and A. annua demonstrated the highest efficacy against first instar larvae of both species, with estimated LC50 values of 84.19 and 76.64 μl/L air, respectively. Following closely, EOs of A. annua and F. gummosa exhibited notable effectiveness against first instar larvae of E. kuehniella, while EOs of M. communis and Z. multiflora showed similar efficacy against first instar larvae of P. interpunctella. Conversely, the EOs of C. limon, T. balsamita, O. majorana and E. persica displayed the least larvicidal activity against E. kuehniella larvae, whereas the EOs of O. majorana and E. persica demonstrated the lowest efficacy against P. interpunctella larvae. Consistent with the findings concerning the eggs, the first instar larvae of P. interpunctella demonstrated slightly greater sensitivity compared to those of E. kuehniella. The EOs exhibited similar lethal effects against adults of both species. Notably, M. communis EO exhibited the highest lethality against male and female adults of both species, followed by EOs of A. annua, E. persica and Z. multiflora. Conversely, EOs of C. limon, T. balsamita, F. gummosa and O. majorana displayed the least lethal effect. Interestingly, female adults showed greater tolerance compared to male adults. Moreover, similar to the observations with eggs and first instar larvae, adults of P. interpunctella displayed slightly greater sensitivity than those of E. kuehniella.

Discussion

The study findings highlight the significant lethal effects of various plant EOs, indicating promising alternatives to hazardous chemical pesticides. Iran's rich pharmaceutical plant flora contains diverse compounds, including volatile ones like EOs, which can be explored for their medicinal, insecticidal, fungicidal and other properties. The availability of formulations derived from complete plant EOs or their active components (i.e. insecticides, acaricides, fungicides and herbicides) in the market suggests the potential for developing more potent and environmentally friendly biorational pesticides through dedicated research in this field.

Keywords

Main Subjects


Abbott, W. S. (1925). A method of computing the effectiveness of an insecticide. Journal of Economic Entomology, 18(2), 265-267.
Abdelgaleil, S. A. M., Mohamed, M. I. E., Badawy, M. E. I., & El-Arami, S. A. A. (2009). Fumigant and contact toxicities of monoterpenes to Sitophilus oryzae (L.) and Tribolium castaneum (Herbst) and their inhibitory effects on acetylcholinesterase activity. Journal of Chemical Ecology, 35, 225-232. https://doi.org/10.1007/s10886-009-9635-3.
Abdelgaleil, S. A. M., Mohamed, M. I. E., Shawir, M. S., & Abou-Taleb, H. K. (2016). Chemical composition, insecticidal and biochemical effects of essential oils of different plant species from Northern Egypt on the rice weevil, Sitophilus oryzae L. Journal of Pest Science, 89(1), 219-229. https://doi.org/10.1007/s10340-015-0665-z.
Ahmadi, Z., Mehrvar, A., & Hassanpouraghdam, M. B. (2014). Study on the effects of four species of essential oils from Petroselium sativum, Ocimum basilicum, Tanacetum balsamita and Cupressus arizonica on first instar larval Ephestia kuehniella Zeller (Lep.: Pyralidae). Proceedings of 21st Iranian Plant Protection Congress. 23-26 August, 2014, Urmia University, Urmia, Iran. p. 540.
Ahsaei, S. A., Rodríguez-Rojo, S., Salgado, M., Cocero, M. J., Talebi-Jahromi, Kh., & Amoabediny, Gh., (2020). Insecticidal activity of spray dried microencapsulated essential oils of Rosmarinus officinalis and Zataria multiflora against Tribolium confusum. Crop Protection, 128, 104996. https://doi.org/10.1016/j.cropro.2019.104996.
Amoura, M., Benabdallah, A., Kilani-Morakchi, S., & Messaoud, C. (2021). Fumigant and repellent potentials of Mentha pulegium L. and Citrus limon L. (Burm) essential oils against Tribolium confusum Duval. (Coleoptera: Tenebrionidae). Journal of Entomological Research, 45(1), 73-80. https://doi.org/10.5958/0974-4576.2021.00012.8.
Atik, H., Bülbül, T., Özdemir, V., Avci, G., & Bülbül, A., (2020). Effect of myrtle (Myrtus communis L.) essential oil on oxidant-antioxidant balance in rats with propylthiouracil-induced hypothyroidism. Journal of Food Biochemistry, 00:e13498. https://doi.org/10.1111/ jfbc.13498.
Attighi Lorestani, F., Khashaveh, A., & Attighi Lorestani, R. (2013). Fumigant toxicity of essential oil from Tanacetum balsamita L. (Compositae) against adults and eggs of Callosobruchus maculatus F. (Coleoptera: Bruchidae). Archives of Phytopathology and Plant Protection, 46(17), 2080-2086. https://doi.org/10.1080/03235408.2013.785112.
Aouadi, G., Haouel, S., Soltani, A. Ben Abada, M., Boushih, E., Elkahoui, S., Taibi, F., Ben Jemâa, J. M., & Bennadja, S.  (2020). Screening for insecticidal efficacy of two Algerian essential oils with special concern to their impact on biological parameters of Ephestia kuehniella (Zeller) (Lepidoptera: Pyralidae). Journal of Plant Diseases and Protection, 127, 471-482. https://doi.org/10.1007/s41348-020-00340-y.
Ayvaz, A., Karaborklu, S., & Sagdic, O. (2009). Fumigant toxicity of five essential oils against the eggs of Ephestia  kuehniella and Plodia  interpunctella (Lepidoptera: Pyralidae). Asian Journal of Chemistry, 21(1), 596-604.
Ayvaz, A., Sagdic, O., Karaborklu, S., & Ozturk, I. (2010). Insecticidal activity of the essential oils from different plants against three stored-product insects. Journal of Insect Science, 10: 21. https://doi.org/10.1673/031.010.2101.
Bagci, E., Kursat, M., Kocak, A., & Gur, S. (2008). Composition and antimicrobial activity of the essential oils of Tanacetum balsamita L. subsp. balsamita and T. chiliophyllum (Fisch. et Mey.) Schultz Bip. var. chiliophyllum (Asteraceae) from Turkey. Journal of Essential Oil Bearing Plants, 11(5), 476-484. https://doi.org/10.1080/0972060X.2008.10643656.
Bagheri-Zenouz, E. (2007). Pest of stored products and management to maintain, biology of insects, acari and microorganisms (1st ed.). University of Tehran Press. (In Farsi).
Bughio, F. M., & Wilkins, R.M. (2004). Influence of Malathion resistance status on survival and growth of Tribolium castaneum (Coleoptera: Tenebrionidae), when fed on four from insect-resistant and susceptible grain rice cultivars. Journal of Stored Products Research, 40(1), 65-75. https://doi.org/10.1016/S0022-474X(02)00077-2.
Baj, T., Baryluk, A., & Sieniawska, E. (2018). Application of mixture design for optimum antioxidant activity of mixtures of essential oils from Ocimum basilicum L., Origanum majorana L. and Rosmarinus officinalis L. Industrial Crops and Products, 115, 52-61. https:// doi.org/10.1016/j.indcrop.2018.02.006.
Bouchelos, K. T. (2018). Insects of warehouses and food. Embryo Publications. Athens, Greece. (In Greek).
Benddine, H., Zaid, R., Babaali, J., & Daoudi-Hacini, S. (2023). Biological activity of essential oils of Myrtus communis (Myrtaceae, Family) and Foeniculum vulgare (Apiaceae, Family) on open fields conditions against corn aphids Rhopalosiphum maidis (Fitch, 1856) in western Algeria. Journal of the Saudi Society of Agricultural Sciences, 22(2), 78-88. https:// doi.org/10.1016/j.jssas.2022.07.001.
Bilia, A. R., Santomauro, F., Sacco, C. , Bergonzi, M. C., & Donato, R. (2014). Essential oil of Artemisia annua L.: an extraordinary component with numerous antimicrobial properties. Evidence-Based Complementary and Alternative Medicine, 159819, https://doi.org/10.1155/ 2014/159819.
Bouyahya, A., Mechchate, H., Benali, T., Ghchime, R., Charfi, S., Balahbib, A., Burkov, P., Shariati, M. A., Lorenzo, J. M., & el Omari, N. (2021). Health benefits and pharmacological properties of Carvone. Biomolecules, 11(12),1803. https://doi.org/10.3390/biom11121803.
Bovard, R., Rezazadeh, S. A., Naghavi, M. R., Omidi, M., Torabi, S., Parvane, S., Hariri Akbari, F., & Taghizad Farid, R. (2014). Variation in the essential oil of Artemisia annua L. apical shoots at different developmental stages. Iranian Journal of Horticultural Science, 45(3), 319-324. https://doi.org/10.22059/ijhs.2014.52881. (In Farsi with English summary).
Chaves, R. S. B., Martins, R. L., Rodrigues, A. B. L., Rabelo, E. M., Farias, A. L. F., Brandão, L. B., Santos, L. M., Galardo, A. K. R., & Almeida, S. S. M. S. (2020). Evaluation of larvicidal potential against larvae of Aedes aegypti (Linnaeus, 1762) and of the antimicrobial activity of essential oil obtained from the leaves of Origanum majorana L. PLoS ONE, 15(7), e0235740. https://doi.org/10.1371/journal.pone.0235740.
Deb, M., & Kumar, D. (2020). Bioactivity and efficacy of essential oils extracted from Artemisia annua against Tribolium castaneum (Herbst. 1797) (Coleoptera: Tenebrionidae): An eco-friendly approach. Ecotoxicology and Environmental Safety, 189, 109988, https://doi. org/10.1016/j.ecoenv.2019.109988.
Demeter, S., Lebbe, O., Hecq, F., Nicolis, S. C., Kemene, T. K., Martin, H., Fauconnier, M.-L., & Hance, T. (2021). Insecticidal activity of 25 essential oils on the stored product pest, Sitophilus granarius. Foods, 10(2), 200. https://doi.org/10.3390/foods10020200.
Demirel, N., Sener, O., Arslan, M., Uremis, I., Uluc, F. T., & Cabuk, F. (2009). Toxicological responses of confused flour beetle, Tribolium confusum du val (Coleoptera: Tenebrionidae) to various plant essential oils. Asian Journal of Chemistry, 21(8), 6403-6410.
De-Oliveira, A. C. A. X., Ribeiro-Pinto, L. F., & Paumgartten, F. J. R. (1997). In vi­tro inhibition of CYP2B1 monooxygenase by b-myrcene and other monoterpenoid compounds. Toxicology Letters, 92(1), 39-46. https://doi.org/10.1016/S0378-4274(97)00034-9.
Donato, R., Santomauro, F., Bilia, A. R., Flamini, G., & Sacco, C. (2015). Antibacterial activity of Tuscan Artemisia annua essential oil and its major components against some foodborne pathogens. LWT-Food Science and Technology, 64, 1251-1254. https://doi.org/ 10.1016/j.lwt.2015.07.014.
Ebadollahi, A. (2011). Iranian plant essential oils as sources of natural insecticide agents. International Journal of Biological Chemistry, 5(5), 266-290. https://doi.org/10.3923/ijbc. 2011.266.290.
Ebadollahi, A. A. (2013). Essential oil isolated from Myrtaceae family as natural insecticides. Annual Research and Review in Biology, 3(3), 148-175.
Ebrahimzadeh, H., Yamini, Y., Sefidkon, F., Chaloosi, M., & Pourmortazavi, S. M. (2003). Chemical composition of the essential oil and supercritical CO2 extracts of Zataria multiflora Boiss. Food Chemistry, 83(3), 357-361. https://doi.org/10.1016/S0308-8146(03)00096-7.
Emamjomeh, L., Imani, S., Talebi, Kh., Moharramipour, S. & Larijani, K. (2014). Chemical composition and insecticidal activity of essential oil of Zataria multiflora Boiss. (Lamiaceae) against Ephestia kuehniella (Lepidoptera: Pyralidae). European Journal of Experimental Biology, 4(3), 253-257.
Emamjomeh, L., Imani, S., Talebi, Kh., & Moharramipour ,S. (2021). Nanoencapsulation enhances the contact toxicity of Eucalyptus globulus Labill and Zataria multiflora Boiss essential oils against the third instar larvae of Ephestia kuehniella (Lepidoptera: Pyralidae). International Journal of Pest Management, 69(2),1-9. https://doi.org/10.1080/09670874. 2020.1871529.
Emamjomeh, L., Imani, S., Talebi, K. H., Moharramipour, S., & Larijani, K. (2018). Preparation of nanoemulsion formulation of essential oil of Zataria multiflora and comparison of contact toxicity with pure essential oil on Ephestia kuehniella. Applied Entomology and Phytopathology, 85(2), 181-190. https://doi.org/10.22092/jaep.2017. 109159. 1151. (In Farsi with English summary).
Enan, E. (2001). Insecticidal activity of essential oils: octopaminergic sites of action. Comparative Biochemistry and Physiology Part C: Toxicology and Pharmacology, 130(3), 325-337. https://doi.org/10.1016/S1532-0456(01)00255-1.
Forouzan, M., Hosseinzadeh, A., Aramideh, Sh., Ghassemi-Kahrizeh, A., Mirfakhraie, Sh., & Mahinfar, S. (2016). Fumigant toxicity of essential oils from Artemisia annua L. and the synergistic effect of acetone against three most important stored pests. Journal of Entomology and Zoology Studies, 4(6), 117-120.
Gallori, S., Flamini, G., Bilia, A. R., Morelli, I., Landini, A., & Vincieri, F. F. (2001). Chemical composition of some traditional herbal drug preparations: Essential oil and aromatic water of costmary (Balsamita suaveolens Pers.). Journal of Agricultural and Food Chemistry, 49, 5907-5910. https://doi.org/10.1021/jf0107656.
Gao, Z., Yu, Z., Qiao, Y., Bai, L., Song, X., Shi, Y., Li, X., Pang, B., Ayiguli, M., & Yang, X. (2022). Chemical profiles and enzyme-targeting acaricidal properties of essential oils from Syzygium aromaticum, Ilex chinensis and Citrus limon against Haemaphysalis longicornis (Acari: Ixodidae). Industrial Crops and Products, 188, Part A, 115697, https://doi.org/10. 1016/j.indcrop.2022.115697.
Ghannadi, A., & Amree, S. (2002). Volatile oil constituents of Ferula gummosa Boiss. from Kashan, Iran. Journal of Essential Oil Research, 14, 420-421. https://doi.org/10.1080/ 10412905.2002.9699908.
Ghasemi, V., Khoshnood Yazdi, A., Zaker Tavallaie, f., & Jalali Sendi, J. (2013). Effect of essential oils from Callistemon viminalis and Ferula gummosa on toxicity and on the hemocyte profile of Ephestia kuehniella (Lep.: Pyralidae). Archives of Phytopathology and Plant Protection, 1(1), 1-11. http://dx.doi.org/10.1080/03235408.2013.808856.
Gillvari, A., Hosseini Gezir, A., Panahian, A. R., & Shakeri, R. (2011). Comparative assessment on efficiency and compounds of Ferula gummosa Boiss. essential oils at two different harvesting areas of Alborz mountains in Iran. Planta Medica, 77(12). https://doi. org/10.1055/s-0031-1282348.
Goodarzi, S., Mofasseri, M., Tofighi, Z., Pirali Hamedani, M., Hadjiakhoondi, A., Tavakoli, S., Moein, Z., & Baharipour, Z. (2022). Remarkable variation in phytochemicals of Ferula gummosa Bioss. essential oils collected from different parts of Iran. Research Journal of Pharmacognosy, 9(4), 29-38. https://doi. org/10.22127/rjp.2022.345563.1917.
Gupta, I., Singh, R., Muthusamy, S., Sharma, M., Grewal, K., Singh, H. P., & Batish, D. R. (2023). Plant essential oils as biopesticides: applications, mechanisms, innovations, and constraints. Plants, 12, 2916. https://doi.org/10.3390/plants12162916.
Habibian, S. M. R., Sorbi Akbari, P., & Rowshan, V. (2021). Study on quantitative and qualitative changes in essential oil compounds of Teucrium polium L. subsp. polium at different phenological stages. Iranian Journal of Medicinal and Aromatic Plants Research, 37(2), 229-241. https://doi.org/10.22092/ijmapr.2021.351556.2847. (In Farsi with English summary).
Hadj Larbi, N., Moghrani, H., Nasrallah, N., Benelmouffok, A., & Kellou, D. (2023). Influence of harvest season on the chemical composition and antifungal activity of Citrus limon essential oil. Rendiconti Lincei. Scienze Fisiche e Naturali, 34, 295-303. https://doi. org/10.1007/s12210-023-01132-w.
Harati, H., Narenji Sani, R., Jebelli Javan, A., Ahmadi-Hamedani, M., & Naeimi, S. (2022). Efficacy of Zataria multiflora essential oil for treatment of Staphylococcus aureus detected by polymerase chain reaction in lactating dairy cows with subclinical mastitis. Iranian Veterinary Journal, 18(1), 34-45. https://doi.org/10.22055/ivj.2022.342990.2468.
Hashemi Bidsookhteh, S. Kh. (2018). The effects of eight plant essential oils on some reproductive properties of the Indian meal moth, Plodia interpunctella (Lepidoptera; Pyralidae). [M.Sc. Thesis, Gorgan University of Agricultural Sciences and Natural Resources]. Gorgan, Iran. (In Farsi with English summary).
Hassanpouraghdam, M. B., Tabatabaie, S. J., Nazemyieh, H., Aflatuni, A., & Vojodi, L. (2008a). Essential oil composition of hydroponically grown Chrysanthemum balsamita L. Journal of Essential Oil Bearing Plants, 11(6), 649-654. https://doi.org/10.1080/0972060X. 2008.10643682.
Hassanpouraghdam, M. B., Tabatabaie, S. J., Nazemyieh, H., Vojodi, L., & Aazami, M.A. (2008b). Volatile oil constituents of alecost [Tanacetum balsamita L. ssp. balsamitoides (Schultz-Bip.)] growing wild in North-West of Iran. Herba Polonica, 55(1), 53-59.
Hatamnia, A. A. (2023). Effects of ecological conditions on antioxidant properties, quantity, and quality of Thymbra spicata L. essential oil. Iranian Journal of Medicinal and Aromatic Plants Research, 39(1), 95-105. https://doi.org/10.22092/ijmapr.2022.358971.3183. (In Farsi with English summary).
Hennia, A., Nemmiche, S., Dandlen, S., & Miguel, M.G. (2019). Myrtus communis essential oils: insecticidal, antioxidant and antimicrobial activities: a review. Journal of Essential Oil Research, 31(6), 487-545. https://doi.org/10. 1080/10412905.2019.1611672.
Hojjati, M., & Barzegar, H. (2017). Chemical composition and biological activities of lemon (Citrus limon) leaf essential oil. Nutrition and Food Sciences Research, 4(4), 15-24. https:// doi.org/10.29252/nfsr.4.4.3.
Hosseinpour, M. H., Askarianzadeh, A., Moharramipour, S., & Jalali Sendi, J. (2011). Insecticidal activity of essential oils isolated from Rue (Ruta graveolens L.) and Galbanum (Ferula gummosa Bioss.) on Callosobruchus maculatus (F.). IOBC/wprs Bulletin, 69, 271-275.
Isman, M. B., & Machial, C. M. (2006). Pesticides based on plant essential oils: from traditional practice to commercialization: In M. Rai & M. Carpinella (Eds.). Naturally occurring bioactive compounds (pp. 29-44). Elsevier B.V.
Jacob, P., & Qamar, A. (2013). Reproductive impairment and lethal effects of selected combinations of some essential oils against the rice moth, Corcyra cecphalonica. European Journal of Experimental Biology, 3(3), 409-415.
Hossein Jafari, S., & Saadatfar, A. (2020). Genetic relationship and phytochemical assessment among populations of Bunium persicum (Boiss.) B. Fedtsch. in the natural habitats of Yazd and Kerman. Iranian Journal of Medicinal and Aromatic Plants, 36(2), 305-316. https://doi. org/10.22092/ijmapr.2020.127522.2625. (In Farsi with English summary).
Jaimand, K., & Rezaee, M. B. (2005). Chemical constituents of essential oils from Tanacetum balsamita L. ssp. balsamitoides (Schultz-Bip.) Grierson. from Iran. Journal of Essential Oil Research, 17(5), 565-566. https://doi.org/10.1080/10412905.2005.9698996.
Kakouri, E., Daferera, D., Kanakis, C., Revelou, P. -K., Kaparakou, E. H., Dervisoglou, S., Perdikis, D., & Tarantilis, P. A. (2022). Origanum majorana essential oil- A review of its chemical profile and pesticide activity. Life, 12(12), 1982. https://doi.org/10.3390/life 12121982.
Karabörklü, S., Ayvaz, A., & Yilmaz, S. (2010). Bioactivities of different essential oils against the adults of two stored product insects. Pakistan Journal of Zoology, 42(6), 679-686.
Karabörklü, S., Ayvaz, A., Yilmaz, S., & Akbulut, M. (2011). Chemical composition and fumigant toxicity of some essential oils against Ephestia kuehniella. Journal of Economic Entomology, 104(4), 1212-1219. https://doi.org/10.1603/ec10284 .
Khanavi, M., Laghaei, P., & Isman, M. B. (2017). Essential oil composition of three native Persian plants and their inhibitory effects in the cabbage looper, Trichoplusia ni. Journal of Asia-Pacific Entomology, 20(4), 1234-1240. https://doi.org/10.1016/j.aspen.2017.08.028.
Khani, A., & Basavand, F. (2012). Chemical composition and insecticidal activity of myrtle (Myrtus communis L.) essential oil against two stored-product pests. Journal of Medicinal Plants and By-products, 1(2), 83-89. https://doi.org/10.22092/jmpb.2012.108471.
Khani, M., Marouf, A., Amini, S., Yazdani, D., Farashiani, M., Ahvazi, M., Khalighi-Sigaroodi, F., & Hosseini-Gharalari, A. (2017). Efficacy of three herbal essential oils against rice weevil, Sitophilus oryzae (Coleoptera: Curculionidae). Journal of Essential Oil Bearing Plants, 20(4), 937-950. https://doi.org/10.1080/0972060X.2017.1355748.
Kheirkhah, M., Ghasemi, V., Khoshnood Yazdi, A., & Rahban, S. (2015). Chemical composition and insecticidal activity of essential oil from Ziziphora clinopodioides Lam. used against the Mediterranean flour moth, Ephestia kuehniella Zeller. Journal of Plant Protection Research, 55(3), 260-265. https://doi.org/10.jppr/2015-0037.
Kostyukovsky, M., Rafaeli, A., Gileadi, C., Demchenko, N., & Shaaya, E. (2002). Activation of octopaminergic receptors by essential oil constituents isolated from aromatic plants: Possible mode of action against insect pests. Pest Management Science, 58(11), 1101-1106. https://doi.org/10.1002/ps.548.
Koutsaviti, A., Antonopoulou, V., Vlassi, A., Antonatos, S., Michaelakis, A., Papachristos, D. P., & Tzakou, O. (2018). Chemical composition and fumigant activity of essential oils from six plant families against Sitophilus oryzae (Col: Curculionidae). Journal of Pest Science, 91, 873-886. https://doi.org/10.1007/s10340-017-0934-0.
Kowsari, N., Moazeni, M., & Mohammadi, A. (2021). Effects of Zataria multiflora essential oil on the germinative cells of Echinococcus granulosus. Parasites Vectors, 14, 257, https:// doi.org/10.1186/s13071-021-04765-8.
Mady, H. Y., Ahmed, M. M., & El Namaky, A. H. (2021). Efficiency of Origanum majorana essential oil as insecticidal agent against Rhynchophorus ferrugineus the red palm weevil (Olivier) (Coleoptera: Curculionidae). Journal of Biopesticides, 14(1), 32-40.
Mahmoudvand, M., Abbasipour, H., Basij, M., Hosseinpour, M. H., Rastegar, F., & Nasiri, M. B. (2011). Fumigant toxicity of some essential oils on adults of some stored-product pests. Chelian Journal of Agricultural Research, 71(1), 83-89. https://doi.org/10.4067/S0718-58392011000100010.
Mahmoudvand, M., Abbasipour, H., Rastegar, F., Hosseinpour, M. H., & Basij, M. (2012). Efficacy of some plants as a post-harvest protectant against some major stored pests. Archives of Phytopathology and Plant Protection, 45(7), 806-811. doi:10.1080/03235408.2011. 597151.
Mashhadi, F., Ghorbani Nohooji, M., & Yaraee, R. (2021). Effects of essential oils of Origanum vulgare L. and Origanum majorana L. on cancer cells line BCL-1 and immune system cells. Iranian Journal of Medicinal and Aromatic Plants Research, 37(5), 781-794. https://doi.org/10.22092/ijmapr.2021.352596.2898. (In Farsi with English summary).
Massiha, A., Khoshkholgh-Pahlaviani, M. M., Issazadeh, Kh., Bidarigh, S., & Zarrabi, S. (2012). Antibacterial activity of essential oils and plant extracts of Artemisia (Artemisia annua L.) in vitro. Zahedan Journal of Research in Medical Sciences, 15(6), 14-18.
Miresmailli, S., & Isman, M. B. (2006). Efficacy and persistence of rosemary oil as an acaricide against two-spotted spider mite (Acari: Tetranychidae) on greenhouse tomato. Ecotoxicology, 99(6), 2015-2023. https://doi.org/10.1603/0022-0493-99.6.2015.
Modarres Najafabadi, S. S., Fanai, H. R., & Ghlamian, Gh. (2006). Study on eucalyptus product uses (seed and leaf powder) on stored product pests of wheat and barley in sistan region-Iran. Iranian Journal of Medicinal and Aromatic Plants, 22(2), 117-127. https://doi. org/10.22092/ijmapr.2006.114979. (In Farsi with English summary).
Mohammadhosseini, M., Mahdavi, B., & Shahnama, M. (2015). Chemical composition of essential oils from aerial parts of Ferula gummosa (Apiaceae) in Jajarm region, Iran using traditional hydrodistillation and solvent-free microwave extraction methods: a comparative
approach. Journal of Essential Oil Bearing Plants, 18(6), 1321-1328. https://doi.org/10.1080/ 0972060X.2015.1024445.
Mojarab-Mahboubkar, M., Afrazeh, Z., Azizi, R., & Jalali Sendi, J. (2023). Efficiency of Artemisia annua L. essential oil and its chitosan/tripolyphosphate or zeolite encapsulated form in controlling Sitophilus oryzae L. Pesticide Biochemistry and Physiology, 195, 105544, https://doi.org/10.1016/j.pestbp.2023.105544.
Moravej, G. H., Of-Shahraki, Z., Azizi, M., & Yaghmaee, F. (2009). Fumigant toxicity of Bunium persicum Boiss. (Umbelliferae) and Elletaria cardamomum Maton. (Zingiberaceae) oils against Tribolium castaneum (Herbst.) (Coleoptera: Tenebrionidae). Journal of Iranian Plant Protection Research, 23(2), 96-105. https://doi.org/10.22067/jpp.v23i2.2555. (In Farsi with English summary).
Moreira, M. D., Picanco, M. C., Barbosa, L. C. d. A., Guedes, R. N. C., Campos, M. R. d., Silva, G. A., & Martins, J. C. (2007). Plant compounds insecticide activity against Coleoptera pests of stored products. Pesquisa Agropecuaria Brasileira, 42(7), 909-915. https://doi.org/ 10.1590/s0100-204x2007000700001.
Nosrati Momvandi, M., Zeid Ali, E., Zarea, M. J., Mumivand, H., & Kiani, M. (2021). Effects of planting date, full fertilizer, and harvest time on quantitative and qualitative yield of Satureja rechingeri Jamzad. Iranian Journal of Medicinal and Aromatic Plants Research, 37(2), 242-259. https://doi.org/10.22092/ijmapr.2021.341804.2716.
Nouri Ganbalani, G., Abedi, Z., Mottaghinia, L., & Nouri, A. (2021). Fumigant toxicity and sublethal effects of black cumin (Bunium persicum Boiss.), cinnamon (Cinnamomum zeylanicum Blume), and peppermint (Mentha piperita L.) essential oils against the Angoumois grain moth, Sitotroga cerealella Olivier (Lepidoptera: Gelechiidae). Iranian Journal of Plant Protection Science, 52(1), 53-67. https://doi.org/10.22059/ijpps.2021. 320474.1006971. (In Farsi with English summary).
Partovi, R., Talebi, F., & Sharifzadeh, A. (2018). Antimicrobial efficacy and chemical properties of Caryophyllus aromaticus and Origanum majorana essential oils against foodborne bacteria alone and in combination. International Journal of Enteric Pathogens, 6(4), 95-103. https://doi.org/10.15171/ijep.2018.25.
Pavela, R., Morshedloo, M. R., Lupidi, G., Carolla, G., Barboni, L., Quassinti, L., Bramucci, M., Vitali, L. A., Petrelli, D., Kavallieratos, N. G., Boukouvala, M. C., Ntalli, N., Kontodimas, D. C., Maggi, F., Canale, A., & Benelli, G. (2020). The volatile oils from the oleo-gum-resins of Ferula assa-foetida and Ferula gummosa: A comprehensive investigation of their insecticidal activity and eco-toxicological effects. Food Chemistry and Toxicology, 140, 111312. https://doi.org/10.1016/j.fct.2020.111312.
Paw, M., Begum, T., Gogoi, R., Pandey, S. K., & Lal, M. (2020). Chemical composition of Citrus limon L. Burmf peel essential oil from north east India. Journal of Essential Oil Bearing Plants, 23(2), 337-344. https://doi.org/10.1080/ 0972060X.2020.1757514.
Perinelli, D. R,, Pavela, R., Bonacucina, G., Baldassarri, C., Spinozzi, E., Torresi, J., Petrelli, R., Morshedloo, M. R., Maggi, F., Benelli, G., & Canale, A. (2022).  Development, characterization, insecticidal and sublethal effects of Bunium persicum and Ziziphora clinopodioides-based essential oil nanoemulsions on Culex quinquefasciatus. Industrial Crops and Products, 186, 115249. https://doi.org/10.1016/j.indcrop.2022. 115249.
Prabu, S., Jing, D., Chandran, V., & Mathew, P. (2020). Insecticidal activity of Origanum majorana L. essential oil as anti-cholinergic agent. Entomological Research, 50(8), 402-413. https://doi.org/10.1111/1748-5967.12459.
Rahmat, A., Edrini, S., Ismail, P., Hin, T. Y. Y., & Bakar, M. F. A. B. (2006). Chemical constituents, antioxidant and cytotoxic effects of essential oil from Strobilanthes crispus and Lawsonia inermis. Journal of Biological Sciences, 6(6), 1005-1010. https://doi.org/10.3923/ jbs.2006.1005.1010.
Rastegar, F., Moharramipour, S., Shojai, M., & Abbasipour, H. (2011). Chemical composition and insecticidal activity of essential oil of Zataria multiflora Boiss. (Lamiaceae) against Callosobruchus maculatus (F.) (Coleoptera: Bruchidae). IOBC/wprs Bulletin, 69, 281-288.
Robertson, J. L., Jones, M. M., Olguin, E., & Alberts, B. (2017). Bioassay with arthropods (3rd ed.). CRC Press.
Rozman, V., Kalinovic, I., & Korunic, Z. (2007). Toxicity of naturally occurring compounds of Lamiaceae and Lauraceae to three stored-product insects. Journal of Stored Products Research, 43, 349-355. https://doi.org/10.1016/j.jspr.2006.09.001.
Salahi, F., Mehrvar, S., & Ahani Azad, M. (2012). Study of ovicidal effect of four plant essential oils on Mediterranean flour moth’s (Ephestia kuehniella Zell.) eggs. In A. Sarafrazi, M. R. Asef, M. Mozhdehi, M. Mozhdehi, S. Solhjouy Fard, & T. Abdollahi (Eds.),  Proceedings of 20th Iranian plant protection congress (p. 240). 26-29 August, 2012, Shiraz University, Shiraz, Iran.
Salehi, T., Karimi, J., Hasanshahi, Gh., Askarianzadeh, A., Abbasipour, H., & Sheikhi Garjan, A. (2014). The effect of essential oils from Laurus nobilis and Myrtus commonis on the adults of mediterranean flour moth, Ephestia kuehniella Zeller (Lep.: Pyralidae). Journal of Essential Oil Bearing Plants, 17(4), 553-561. https://doi.org/10.1080/0972060X.2014. 935059.
Seyedi, A., Abbasipour, H., Moharramipour, S., & Kamalinejad, M. (2010). Ovicidal effect of essential oil of Ferula gummosa Boiss on the Mediterranean flour moth Ephestia kuehniella Zeller. In S. Manzari (Ed.), Proceedings of the 19th Iranian plant protection congress, Vol. 1 (Pests) (p. 172). 31 July-3 August 2010, Iranian Research Institute of Plant Protection, Tehran, Iran.
Singh, G., Singh, O. P., De-Lampasona, M. P., & Catalan, C. A. N. (2003). Studies on essential oils. Part 35: chemical and biocidal investigation on Tagetes erecta leaf volatile oil. Flavour and Fragrance Journal, 18(1), 62-65. https://doi.org/10.1002/ffj.1158.
Siyadatpanah, A., Norouzi, R., Mirzaei, F., Haghirosadat, B. F., Nissapatorn, V., Mitsuwan, W., Nawaz, M., Pereira, M. L., Hosseini, S. A., Montazeri, M., Majdizadeh, M., Almeida, R. S., Hemati, M., Wilairatana, P., & Coutinho, H. D. M. (2023). Green synthesis of nano-liposomes containing Bunium persicum and Trachyspermum ammi essential oils against Trichomonas vaginalis. Journal of Microbiology, Immunology and Infection, 56(1), 150-162. https://doi.org/10.1016/j.jmii.2022.06.006.
Sokuti, Y., & Ghasemi, V. (2018). Acute and chronic toxicity of Ziziphora clinopodioides and Ferula gummosa essential oils against Plodia interpunctella (Lepidoptera: Pyralidae). Journal of Entomological Society of Iran, 38(2), 187-203. https://doi.org/10.22117/jesi.2018.120696. 1195.
Sousa, P. A. S., Netoa, J., Bastos, M. M. S. M., & Aguiar, A. A. R. M. (2022). Eugenol and Pulegone as potential biorational alternatives for Trioza erytreae (Hemiptera: Triozidae) control: Preliminary results on nymphal toxicity and applicability on Citrus limon. Journal of Natural Pesticide Research, 1, 100004. https://doi.org/10.1016/j.napere.2022.100004.
Stathas, I. G., Sakellaridis, A. C., Papadelli, M., Kapolos, J., Papadimitriou, K., & Stathas, G. J. (2023). The effects of insect infestation on stored agricultural products and the quality of food. Foods, 12, 2046. https://doi.org/10.3390/foods12102046.
Sun, Y. P. (1950). Toxicity index- an improved method of comparing the relative toxicity of insecticides. Journal of Economic Entomology, 43(1), 45-53. https://doi.org/10.1093/jee/43. 1.45.
Tapondjou, A. L., Adler, C., Fontem, D. A., Bouda, H., & Reichmuth, C. (2005). Bioactivities of cymol and essential oils of Cupressus sempervirens and Eucalyptus saligna against Sitophilus zeamais Motschulsky and Tribolium confusum du Val. Journal of Stored Products Research, 41(1), 91-102. https://doi.org/10.1016/j.jspr.2004.01.004.
Theou, G., Papachristos, D. P. and Stomopolos, D .C. (2013). Fumigant toxicity of six essential oils to the immature stages and adults of Tribolium confusum. Hellenic Plant Protection Journal, 6(1), 29-39.Tripathi, A. K., Prajapati, V., Aggarwal, K. K., Khanuja, S. P. S., & Kumar, S. (2000). Repellency and toxicity of oil from Artemisia annua to certain stored-product beetles. Journal of Economic Entomology, 93(1), 43-47. https://doi,org/10.1603/0022-0493-93.1.43.Tsao, R., & Coats, J. R. (1995). Starting from natural to make better in­secticides. Chemtech, 25, 23-28.
Vukic, M. D., Vukovic, N. L., Obradovic, A. D., Galovičová, L., Čmiková, N., Kačániová, M., & Matic, M. M. (2022). Chemical composition and biological activity of Tanacetum balsamita essential oils obtained from different plant organs. Plants, 11(24), 3474. https://doi. org/10.3390/plants11243474.
Weyerstahl, P., Marschall, H., & Rustaiyan, A. (1994). Constituents of the essential oil of Myrtus communis L. from Iran. Flavour and Fragrance Journal, 9(6), 333-337. https://doi. org/10.1002/ffj.2730090610.
Yadav, A., Kumar, A., Singh, P. P, & Prakash, B. (2021). Pesticidal efficacy, mode of action and safety limits profile of essential oils based nanoformulation against Callosobruchus chinensis and Aspergillus flavus. Pesticide Biochemistry and Physiology, 175, 104813, https:// doi.org/10.1016/j.pestbp.2021.104813.
Yazdanian, M., & Reihani, M. (2021). Chemical composition of myrtle essential oil and its insecticidal activity in combination with diatomaceous earth against adults of the granary weevil, Sitophilus granarius (L.). Journal of Plant Protection, 35(2), 203-216. https://doi.org/ 10.22067/jpp.2021.69214.1015. (In Farsi with English summary).
Yousefi, B., Sefidkon, F., Mirza, M., & Lebaschy, M. H. (2022). Effects of different planting densities and feeding with organic fertilizers on percentage, yield, and essential oil chemical composition in Satureja mutica Fisch. & C.A. Mey. under rainfed conditions. Iranian Journal of Medicinal and Aromatic Plants Research, 38(1), 102-113. https://doi.org/10.22092/ijmapr. 2021.354198.2976. (In Farsi with English summary).
Yousefzadi, M., Ebrahimi, S. N., Sonboli, A., Miraghasi, F., Ghiasi, S., Arman, M., & Mosaffa, N. (2009). Cytotoxicity, antimicrobial activity and composition of essential oil from Tanacetum balsamita L. subsp. balsamita. Natural Product Communications, 4(1), 119-122.
Zamani, S., Sendi, J.J., & Ghadamyari, M. (2011). Effect of Artemisia annua L. (Asterales: Asteraceae) essential oil on mortality, development, reproduction and energy reserves of Plodia interpunctella (Hübner). (Lepidoptera: Pyralidae). Journal of Biofertilizers and Biopesticides, 2, 105. https://doi:10.4172/2155-6202.1000105
Zarrad, K., Chaieb, I., Tayeb, W., Chraief, I., Laarif, A., Hammami, M., & Haouala, R. (2013). Bio-insecticidal potential of essential oils of two Citrus species against two greenhouse pests Tuta absoluta Meyrick and Spodoptora littoralis Boisduval. Microbiologie et Hygiène Alimentaire, 25(73), 84-88.
Zayed, G. M. M. (2018). Efficacy of marjoram (Origanum majorana) on Rhizopertha dominica and identification of its chemical components. Academia Journal of Agricultural Research, 6(5), 163-170. https://doi.org/10.15413/ajar.2017.IECCNA.16.
Zomorodian, K., Moein, M., Goeini Lori, Z., Ghasemi, Y., Rahimi, M. J., Bandegani, A., Pakshir, K., Bazargani, A., Mirzamohammadi, S., & Abbasi, N. (2013). Chemical composition and antimicrobial activities of the essential oil from Myrtus communis leaves. TEOP, 16(1), 76-84. https://doi.org/10.1080/0972060X.2013.764183.
 © 2024 by the authors. Licensee SCU, Ahvaz, Iran. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution-NonCommercial 4.0 International (CC BY-NC 4.0 license) (http://creativecommons.org/licenses/by-nc/4.0/.