Abstract
The main objective of the present study is to investigate the fumigant toxicity of EOs extracted from Satureja alpina (L.) Scheele (Lamiaceae), Rosmarinus officinalis (L.) (Lamiaceae) and Ammodaucus leucotrichus (Coss. & Durieu) (Apiaceae) and to predict specific EO mixtures that provide optimal insecticidal activities against two common secondary insect pests, namely Stegobium paniceum (L.) (Coleoptera: Anobiidae) and Tribolium confusum du Val (Coleoptera: Tenebrionidae). GC/MS analysis showed that A. leucotrichus EO was characterized by the abundance of L-perillaldehyde and D-limonene, while the main constituents of R. officinalis EO were 1.8-cineole, camphor, and α-pinene. S. alpina EO was mainly composed of pulegone. Concerning the insecticidal activity, the results showed that all EOs tested individually exerted high efficacy, with LC50 from 3.4 to 6.6 µL/L air for S. paniceum, and from 25.3 to 41.9 µL/L air for T. confusum. The various combinations of these EOs were generally found to possess greater activity than when used individually, and synergistic interactions were recorded. The optimal mixtures predicted were 48% S. alpina, 31% R. officinalis and 21% A. leucotrichus EOs, corresponding to LC50 of 1.47 µL/L air; and 57% A. leucotrichus and 43% S. alpina EOs corresponding to LC50 of 8.26 µL/L air, for S.paniceum and T. confusum, respectively. Our findings showed that the use of these optimized EO combinations from the tested plants could be a promising insecticidal alternative to reduce the use of harmful synthetic insecticides.
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Abbassy MA, Abdelgaleil SAM, Rabie RYA (2009) Insecticidal and synergistic effects of Majorana hortensis essential oil and some of its major constituents. Entomol Exp Appl 131:225–232. https://doi.org/10.1111/j.1570-7458.2009.00854.x
Abbott WS (1925) A method of computing the effectiveness of an insecticide. J Am Mosq Control Assoc 18:265–267
Abdelgaleil SAM, Badawy MEI, Mahmoud NF, Marei AESM (2019) Acaricidal activity, biochemical effects and molecular docking of some monoterpenes against two-spotted spider mite (Tetranychus urticae Koch). Pestic Biochem Physiol 156:105–115. https://doi.org/10.1016/j.pestbp.2019.02.006
Angelini LG, Carpanese G, Cioni PL, Morelli I, Macchia M, Flamini G (2003) Essential oils from Mediterranean Lamiaceae as weed germination inhibitors. J Agric Food Chem 51:6158–6164. https://doi.org/10.1021/jf0210728
Atwood LW, Mortensen DA, Koide RT, Smith RG (2018) Evidence for multi-trophic effects of pesticide seed treatments on non-targeted soil fauna. Soil Biol Biochem 125:144–155. https://doi.org/10.1016/j.soilbio.2018.07.007
Bellakhdar J (2006) Medicinal plants in North Africa and basic care, handbook of modern herbal medicine. Le Fennec, Casablanca
Benchikha N, Rebiai A, Brahmia O, Neghmouche NS, Ben Amor ML (2019) Chemical composition, antimicrobial, antioxidant and anticancer activities of essential oil from Ammodaucus leucotrichus Cosson & Durieu (Apiaceae) growing in south Algeria Benchikha. Bull Chem Soc Ethiop 33:541–549
Boraei DM (2016) Toxicity of two fixed plant oils by using a new fumigant method against Trogoderma granarium Everts and Stegopium paniceum (L.). J Plant Prot Pathol 7(12):791–796
Box GEP (1964) An Introduction to Response Surface Methodology. Madison
Cabrera BJ (2002) Drugstore Beetle, Stegobium paniceum (L.) (Insecta: Coleoptera: Anobiidae). University Life Science of Florida/ Institute of Food and Agricultural Sciences Extension. https://doi.org/10.32473/edis-in385-2001
Choi WS, Park BS, Lee YH, Jang DY, Yoon HY, Lee SE (2006) Fumigant toxicities of essential oils and monoterpenes against Lycoriella mali adults. Crop Prot 25:398–401. https://doi.org/10.1016/j.cropro.2005.05.009
Chou TC (2006) Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol Rev 58:621–681. https://doi.org/10.1124/pr.58.3.10
Crespo YA, Bravo Sanchez LM, Quintana YG, Cabrera AST, del Sol AB, Mayancha DMG (2019) Evaluation of the synergistic effects of antioxidant activity on mixtures of the essential oil from Apium graveolens L., Thymus vulgaris L. and Coriandrum sativum L. using simplex-lattice design. Heliyon 5:e01942. https://doi.org/10.1016/10.1016/j.heliyon.2019.e01942
Daglish GJ, Nayak MK, Arthur Frank H, Athanassiou Christos G (2018) Insect pest management in stored grain. In: Athanassiou CG, Arthur FH (eds) Recent Advances in Stored Product Protection. Springer, Heidelberg, pp 45–63. https://doi.org/10.1007/978-3-662-56125-6_3
El-Bakry AM, Youssef HF, Abdel-Aziz NF, Sammour EA (2019) Insecticidal potential of Ag-loaded 4A-zeolite and its formulations with Rosmarinus officinalis essential oil against rice weevil (Sitophilus oryzae) and lesser grain borer (Rhyzopertha Dominica). J Plant Prot Res 59:324–333. https://doi.org/10.24425/jppr.2019.129741
Elamrani A, Zrira S, Benjilali B, Berrada M (2000) A study of moroccan rosemary oils. J Essent Oil Res 12:487–495. https://doi.org/10.1080/10412905.2000.9699572
El Hidar N, Soulaimani B, André G, Jurgen AB, Abbad A, Hassani L, Mezrioui N (2021) Chemical composition, antibacterial activity and effect of Rhus albida Schousb essential oil on the inhibition of NorA ef fl ux pump in Staphylococcus aureus. South African J Bot 142:19–24. https://doi.org/10.1016/j.sajb.2021.05.025
Fadil M, Fikri-Benbrahim K, Rachiq S, Ihssane B, Lebrazi S, Chraibi M, Haloui T, Farah A (2018) Combined treatment of Thymus vulgaris L., Rosmarinus officinalis L. and Myrtus communis L. essential oils against Salmonella typhimurium: Optimization of antibacterial activity by mixture design methodology. Eur J Pharm Biopharm 126:211–220. https://doi.org/10.1016/j.ejpb.2017.06.002
Fadli M, Chevalier J, Saad A, Mezrioui NE, Hassani L, Pages JM (2011) Essential oils from Moroccan plants as potential chemosensitisers restoring antibiotic activity in resistant Gram-negative bacteria. Int J Antimicrob Agents 38:325–330. https://doi.org/10.1016/j.ijantimicag.2011.05.005
Feroz A (2020) Efficacy and cytotoxic potential of deltamethrin, essential oils of Cymbopogon citratus and Cinnamonum camphora and their synergistic combinations against stored product pest, Trogoderma Granarium. J Stored Prod Res 87:101614. https://doi.org/10.1016/j.jspr.2020.101614
Finney DJ (1971) Probit analysis. 3rd ed, Cambridge
Gallardo A, Picollo MI, Mougabure-Cueto G (2015) Lethal activity of individual and mixed monoterpenoids of geranium essential oil on Musca domestica. Parasitol Res 114:1229–1232. https://doi.org/10.1007/s00436-015-4315-4
Goupy J, Creighton L (2006) Introduction aux plans d’experiences. 3éme édn. Dunod, Paris
Goupy J, Creighton L (2007) Introduction to Design of Experiments with JMP Examples. 3rd edn. Perfect Paperback
Hagstrum DW, Subramanyam B (2009) A review of stored-product entomology information sources. Am Entomol 55:174–183
Halla N, Heleno SA, Costa P et al (2018) Chemical profile and bioactive properties of the essential oil isolated from Ammodaucus leucotrichus fruits growing in Sahara and its evaluation as a cosmeceutical ingredient. Ind Crops Prod 119:249–254. https://doi.org/10.1016/j.indcrop.2018.04.043
Hussein HS (2017) Behavioral and insecticidal effects of three plant oils on bemisia tabaci. J Entomol 14:87–95. https://doi.org/10.3923/je.2017.87.95
Isikber AA, Alma MH, Kanat M, Karci A (2006) Fumigant toxicity of essential oils from Laurus nobilis and Rosmarinus officinalis against all life stages of Tribolium confusum. Phytoparasitica 34:167–177. https://doi.org/10.1007/BF02981317
Isman MB (2000) Plant essential oils for pest and disease management. Crop Prot 19:603–608. https://doi.org/10.1016/s0261-2194(00)00079-x
Jennan S, Fouad R, Nordine A et al (2018) Chemical composition and antibacterial screening of aerial parts of essential oils of three Satureja species (Satureja briquetti, Satureja atlantica and Satureja alpina) Growing Wild in the Middle Atlas Mountains of Morocco. J Essent Oil-Bearing Plants 21:741–748. https://doi.org/10.1080/0972060X.2018.1486230
Jyoti SNK, Singh H, Mehta N, Rath SS (2019) In vitro assessment of synergistic combinations of essential oils against Rhipicephalus (Boophilus) microplus (Acari: Ixodidae). Exp Parasitol 201:42–48. https://doi.org/10.1016/j.exppara.2019.04.007
Kasrati A, Alaoui Jamali C, Bekkouche K, Spooner-Hart R, Leach D, Abbad A (2015) Chemical characterization and insecticidal properties of essential oils from different wild populations of Mentha suaveolens subsp. timija (BRIQ.) HARLEY from Morocco. Chem Biodivers 12:823–831. https://doi.org/10.1002/cbdv.201400236
Kiran S, Kujur A, Patel L, RamalakshmiK PB (2017) Assessment of toxicity and biochemical mechanisms underlying the insecticidal activity of chemically characterized Boswellia carterii essential oil against insect pest of legume seeds. Pestic Biochem Physiol 139:17–23. https://doi.org/10.1016/j.pestbp.2017.04.004
Laghzaoui EM, Kasrati A, Abbad A, Leach D, Spooner-Hart R, El Mouden EH (2018) Acaricidal properties of essential oils from Moroccan plants against immature ticks of Hyalomma aegyptium (Linnaeus, 1758): an external parasite of the spur-thighed tortoise (Testudo graeca). Int J Acarol 44:315–321. https://doi.org/10.1080/01647954.2018.1520918
Lahlou M, Berrada R (2003) Composition and niticidal activity of essential oils of three chemotypes of Rosmarinus officinalis L. acclimatized in Morroco. Flavour Fragr J 18:124–127. https://doi.org/10.1002/ffj.1160
Lazcano Díaz E, Padilla Camberos E, Castillo Herrera GA et al (2019) Development of essential oil-based phyto-formulations to control the cattle tick Rhipicephalus microplus using a mixture design approach. Exp Parasitol 201:26–33. https://doi.org/10.1016/j.exppara.2019.04.008
Liska A, Rozman V, Kalinovic I, Ivezic M, Balicevic R (2010) Contact and fumigant activity of 1,8-cineole, eugenol and camphor against Tribolium castaneum (Herbst). Julius-Kühn-Archiv 425:716–720. https://doi.org/10.5073/jka.2010.425.093
Ma S, Jia R, Guo M, Qin K, Zhang L (2020) Insecticidal activity of essential oil from Cephalotaxus sinensis and its main components against various agricultural pests. IndCrops Prod 150:112403. https://doi.org/10.1016/j.indcrop.2020.112403
Ngassoum MB, Ngamo Tinkeub LS, Ngatankoc I et al (2007) Chemical composition, insecticidal effect and repellent activity of essential oils of three aromatic plants, alone and in combination, towards Sitophilus oryzae L. (Coleoptera: Curculionidae). Nat Prod Commun 2:1229–1232. https://doi.org/10.1177/1934578X0700201207
Novato TPL, Araújo LX, de Monteiro CMO et al (2015) Evaluation of the combined effect of thymol, carvacrol and (E)-cinnamaldehyde on Amblyomma sculptum (Acari: Ixodidae) and Dermacentor nitens (Acari: Ixodidae) larvae. Vet Parasitol 212:331–335. https://doi.org/10.1016/j.vetpar.2015.08.021
Okoh OO, Sadimenko AP, Afolayan AJ (2010) Comparative evaluation of the antibacterial activities of the essential oils of Rosmarinus officinalis L. obtained by hydrodistillation and solvent free microwave extraction methods. Food Chem 120:308–312. https://doi.org/10.1016/j.foodchem.2009.09.084
Oliveira CM, Auad AM, Mendes SM, Frizzas MR (2014) Crop losses and the economic impact of insect pests on Brazilian agriculture. Crop Prot 56:50–54. https://doi.org/10.1016/j.cropro.2013.10.022
Ouedrhiri W, Balouiri M, Bouhdid S et al (2016) Mixture design of Origanum compactum, Origanum majorana and Thymus serpyllum essential oils: Optimization of their antibacterial effect. Ind Crops Prod 89:1–9. https://doi.org/10.1016/j.indcrop.2016.04.049
Pandiyan GN, Mathew N, Munusamy S (2019) Larvicidal activity of selected essential oil in synergized combinations against Aedes aegypti. Ecotoxicol Environ Saf 174:549–556. https://doi.org/10.1016/j.ecoenv.2019.03.019
Park IK, Kim LS, Choi IH, Lee YS, Shin SC (2006) Fumigant activity of plant essential oils and components from Schizonepeta tenuifolia against Lycoriella ingenua (Diptera: Sciaridae). J Econ Entomol 99:1717–1721. https://doi.org/10.1093/jee/99.5.1717
Pavela R, Maggi F, Cianfaglione K, Canale E, Benelli G (2020) Promising insecticidal efficacy of the essential oils from the halophyte Echinophora spinosa (Apiaceae) growing in Corsica Island. France Environ Sci Pollut Res 27:14454–14464. https://doi.org/10.1007/s11356-019-04980-y
Pimentel D (1991) World resources and food losses to pests. In: Gorham JR (ed) Ecology and Management of Food Industry Pests. Association of Official Analytical Chemists, Arlington, MA, USA, pp 5–11
Radhika SA, Sahayaraj K (2016) Insecticidal activity of monocrotophos and pungam oil combinations for cotton pests management under laboratory condition. Agron Trop 66:125–133
Regnault-Roger C, Vincent C, Arnason JT (2012) Essential oils in insect control: Low-risk products in a high-stakes world. Annu Rev Entomol 57:405–424. https://doi.org/10.1146/annurev-ento-120710-100554
Rossi YE, Canavoso L, Palacios SM (2012) Molecular response of Musca domestica L. to Mintostachys verticillata essential oil, (4R)(+)-pulegone and menthone. Fitoterapia 83:336–342. https://doi.org/10.1016/j.fitote.2011.11.019
Sadaoui N, Bec N, Barragan-Montero V et al (2018) The essential oil of Algerian Ammodaucus leucotrichus Coss. & Dur. and its effect on the cholinesterase and monoamine oxidase activities. Fitoterapia 130:1–5. https://doi.org/10.1016/j.fitote.2018.07.015
Sarma R, Adhikari K, Mahanta S, Khanikor B (2019) Combinations of plant essential oil based terpene compounds as larvicidal and adulticidal agent against Aedes aegypti (Diptera: Culicidae). Sci Rep 9:1–12. https://doi.org/10.1038/s41598-019-45908-3
Scalerandi E, Flores GA, Palacio M et al (2018) Understanding synergistic toxicity of terpenes as insecticides: Contribution of metabolic detoxification in Musca domestica. Front Plant Sci 871:1–9. https://doi.org/10.3389/fpls.2018.01579
Sfara V, Zerba EN, Alzogaray RA (2009) Fumigant insecticidal activity and repellent effect of five essential oils and seven monoterpenes on first-instar nymphs of Rhodnius prolixus. J Med Entomol 46:511–515. https://doi.org/10.1603/033.046.0315
Shaaya E, Rafaeli A (2007) Essential oils as biorational insecticides–potency and mode of action. In: Shaaya I, Nauen R, Horowitz AR (eds) Insecticides Design Using Advanced Technologies. Springer, Heidelberg, pp 249–261
Soulaimani B, El Hidar N, Ben Fakir S, Mezrioui NE, Hassani L, Abbad A (2021a) Combined antibacterial activity of essential oils extracted from Lavandula maroccana (Murb.), Thymus pallidus Batt. and Rosmarinus officinalis L. against antibiotic-resistant Gram-negative bacteria. Eur J Integr Med 101312. https://doi.org/10.1016/j.eujim.2021a.101312
Soulaimani B, Nafis A, Kasrati A, Rochdi A, Mezrioui NE, Abbad A, Hassani L (2019) Chemical composition, antimicrobial activity and synergistic potential of essential oil from endemic Lavandula maroccana (Mill.). South African J Bot 125:202–206. https://doi.org/10.1016/j.sajb.2019.07.030
Soulaimani B, Varoni E, Iriti M, Mezrioui NE, Hassani L, Abbad A (2021b) Synergistic anticandidal effects of six essential oils in combination with fluconazole or amphotericin b against four clinically isolated candida strains. Antibiotics 10:1049. https://doi.org/10.3390/antibiotics10091049
Talbaoui A, Jamaly N, Aneb M et al (2012) Chemical composition and antibacterial activity of essential oils from six Moroccan plants. J Med Plants Res 6:4593–4600. https://doi.org/10.5897/jmpr10.078
Togola A, Seck PA, Glitho IA, Diagne A, Adda C, Toure A, Nwilene FE (2013) Economic losses from insect pest infestation on rice stored on-farm in benin. J Appl Sci 13:278–285. https://doi.org/10.3923/jas.2013.278.285
Wittstock U, Gershenzon J (2002) Constitutive plant toxins and their role in defense against herbivores and pathogens. Curr Opin Plant Biol 5:300–307. https://doi.org/10.1016/S1369-5266(02)00264-9
Wu L, Huo X, Zhou X et al (2017) Acaricidal activity and synergistic effect of thyme oil constituents against carmine spider mite (Tetranychus Cinnabarinus (Boisduval)). Molecules 22:1–12. https://doi.org/10.3390/molecules22111873
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We thank the “Haut Commissariat aux Eaux et Forêts et à la Lutte Contre la Désertication (HCEFLCD)” for permission to collect the plant materials from the field.
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B S and E-M L: Laboratory work; M A-B and R S–H: Mixture design and statistical analysis; AA and L H: Collection of plant materials and data analysis. The first version of the present manuscript was written by Bouchra Soulaimani and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Soulaimani, B., Laghzaoui, EM., Babram, M.A. et al. Optimization of the insecticidal response of combined essential oils from Satureja alpina, Rosmarinus officinalis and Ammodaucus leucotrichus using a designed mixtures approach. Int J Trop Insect Sci 42, 2501–2512 (2022). https://doi.org/10.1007/s42690-022-00778-7
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DOI: https://doi.org/10.1007/s42690-022-00778-7