Abstract
Tuta absoluta Meyrick originates in South America and is now one of the most important insect pests of Solanaceae in different parts of the world, including Africa. Its control has relied primarily on chemical insecticides, which are associated with negative ecological effects. In the present study, essential oils of Ocimum gratissimum and O. kilimandscharicum were tested for repellence and fumigant toxicity on the adult stages under laboratory conditions. The oil of O. gratissimum was more repellent, but its toxicity was comparable with that of O. kilimandscharicum. The major constituents of O. gratissimum were methyl eugenol (39.5%) and eugenol (29.7%). Those of O. kilimandscharicum were camphor (47.1%) and 1.8-cineole (19.3%). Eugenol (LC50 of 0.24 μl/ml, 83.3%, RI50 = 0.15) and camphor (LC50 of 0.23 μl/ml, 89.5%, RI50 = 0.13) were more toxic (at 1 μl/ml for 24 h) and repellent than the other constituents. The results show potential of the essential oils for use in integrated management of the tomato pest.
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Abbes K, Chermiti B (2012) Failure of the biological control of Tuta absoluta using the predator Nesidiocoris tenuis in a protected tomato crop: analysis of factors. IOBC/WPRS Bull 80:231–236
Adams RP (2017) Identification of essential oil components by gas chromotography/mass spectrometry, 4th edn. Allured publishing, Carol Stream
Aggarwal KK, Tripathi AK, Prajapati V, Kumar S (2001) Toxicity of 1,8-cineole towards three species of stored product coleopterans. Int J Insect Sci 21:155–160
Ajayi OE, Appel AG, Fadamiro HY (2014) Fumigation toxicity of essential oil monoterpenes to Callosobruchus maculatus (Coleoptera: Chrysomelidae: Bruchinae). J Insects:1–7. https://doi.org/10.1155/2014/917212
Asawalam EF, Emosairue SO, Hassanali A (2008) Essential oil of Ocimum gratissimum (Labiatae) as Sitophilus zeamais (Coleoptera: Curculionidae) protectant. Afr J Biotechnol 7:3771–3776
Beatovic D, Krstić-Milošević D, Trifunovic S, Petrovic J, Glamoclija JM, Ristic M, Jelacic S (2015) Chemical composition, antioxidant and antimicrobial activities of the essential oils of twelve Ocimum basilicum L. cultivars grown in Serbia. Rec Nat Prod 9:62–75
Bekele J, Hassanali A (2001) Blend effects in the toxicity of the essential oil constituents of Ocimum kilimandscharicum and Ocimum kenyense (Labiatae) on two post-harvest insect pests. Phytochemistry 57:385–391
Benelli G, Pavela R, Giordani C, Casettari L, Curzi G, Cappellacci L, Petrelli R, Maggi F (2018) Acute and sub-lethal toxicity of eight essential oils of commercial interest against the filariasis mosquito Culex quinquefasciatus and the housefly Musca domestica. Ind Crop Prod 112:668–680
Benelli G, Pavela R, Maggi F, Wandjou JGN, Fofie NBY, Koné-Bamba D, Sagratini G, Vittori S, Caprioli G (2019) Insecticidal activity of the essential oil and polar extracts from Ocimum gratissimum grown in Ivory Coast: efficacy on insect pests and vectors and impact on non-target species. Ind Crop Prod 132:377–385. https://doi.org/10.1016/j.indcrop.2019.02.047
Bhardwaj A, Tewary DK, Kumar R, Kumar V, Sinha AK, Shanker A (2010) Larvicidal and structure–activity studies of natural phenylpropanoids and their semisynthetic derivatives against the tobacco armyworm Spodoptera litura (Fab.) (Lepidoptera: Noctuidae). Chem Biodivers 7:168–177
Biondi A, Guedes RNC, Wan FH, Desneux N (2018) Ecology, worldwide spread, and management of the invasive south American tomato pinworm, Tuta absoluta: past, present, and future. Annu Rev Entomol 63:239–258. https://doi.org/10.1146/annurev-ento-031616-034933
Biratu W (2018) Review on the effect of climate change on tomato (Solanum lycopersicon) production in Africa and mitigation strategies. J Nat Sci Res 8:62–70
Bissinger BW, Roe RM (2010) Tick repellents: past, present, and future. Pestic Biochem Physiol 96:63–79
Campolo O, Cherif A, Ricupero M, Siscaro G, Grissa-Lebdi K, Russo A, Cucci LM, Pietro PD, Satriano C, Desneux N, Biondi A, Zappalà L, Palmeri V (2017) Citrus peel essential oil nanoformulations to control the tomato borer, Tuta absoluta: chemical properties and biological activity. Sci Rep 7(1):13036. https://doi.org/10.1038/s41598-017-13413-0
Charles DJ, Simon JE (1992) Essential oil constituents of Ocimum kilimandscharicum Guerke. J Essent Oil Res 4:125–128
Chegini SG, Abbasipour H, Karimi J, Askarianzadeh A (2018) Toxicity of Shirazi thyme, Zataria multiflora essential oil to the tomato leaf miner, Tuta Absoluta (Lepidoptera: Gelechiidae). Int J Trop Insect Sci 38:340–347
Chen HP, Yang K, You CX, Lei N, Sun RQ, Geng ZF, Ma P, Cai Q, Du SS, Deng ZW (2014) Chemical constituents and insecticidal activities of the essential oil of Cinnamomum camphora leaves against Lasioderma serricorne. J Chem 2014:1–5. https://doi.org/10.1155/2014/963729
Chowdhary K, Kumar A, Sharma S, Pathak R, Jangir M (2018) Ocimum sp.: source of biorational pesticides. Ind Crop Prod 122:686–701. https://doi.org/10.1016/j.indcrop.2018.05.068
Clemente S, Mareggiani G, Broussalis A, Martino V, Ferraro G (2003) Insecticidal effects of Lamiaceae species against stored products insects. Bol San Veg Plagas 29:421–426
Corbet SA, Danahar GW, King V, Chalmers CL, Tiley CF (1995) Surfactant-enhanced essential oils as mosquito larvicides. Entomol Exp Appl 75:229–236
Cruz GS, Wanderley-Teixeira V, da Silva LM, Dutra KA, Guedes CA, de Oliveira JV, Ferraz Navarro DMA, Araújo BC, Teixeira ÁAC (2017) Chemical composition and insecticidal activity of the essential oils of Foeniculum vulgare Mill., Ocimum basilicum L., Eucalyptus staigeriana F. Muell. ex Bailey, Eucalyptus citriodora Hook and Ocimum gratissimum L. and their major components on Spodoptera frugiperda (Lepidoptera: Noctuidae). J Essent Oil Bear Plants 20:1360–1136
del Toro-Sánchez CL, Ayala-Zavala JF, Machi L, Santacruz H, Villegas-Ochoa MA, Alvarez-Parrilla E, González-Aguilar GA (2010) Controlled release of antifungal volatiles of thyme essential oil from β-cyclodextrin capsules. J Incl Phenom Macro 67:431–441
Desneux N, Decourtye A, Delpuech JM (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106
Desneux N, Wajnberg E, Wyckhuys KAG, Burgio G, Arpaia S, Narváez-Vasquez CA, González-Cabrera J, Ruescas DC, Tabone E, Frandon J, Pizzol J, Poncet C, Cabello T, Urbaneja A (2010) Biological invasion of European tomato crops by Tuta absoluta: ecology, geographic expansion and prospects for biological control. J Pest Sci 83:197–215
Desneux N, Luna MG, Guillemaud T, Urbaneja A (2011) The invasive south American tomato pinworm, Tuta absoluta, continues to spread in Afro-Eurasia and beyond: the new threat to tomato world production. J Pest Sci 84:403–408
Faria TJ, Ferreira RS, Yassumoto L, Pinto de Souza JR, Ishikawa NK, Barbosa AM (2006) Antifungal activity of essential oil isolated from Ocimum gratissimum L. (eugenol chemotype) against phytopathogenic fungi. Braz Arch Biol Technol 49:867–871
Garcia MF, Espul JC (1982) Bioecology of the tomato moth (Scrobipalpula absoluta) in Mendoza, Argentine Republic. Rev Investig Agropecu 17:135–146
Gikonyo NK, Hassanali A, Njagi PGN, Saini RK (2003) Responses of Glossina morsitans morsitans to blends of electroantennographically active compounds in the odors of its preferred (buffalo and ox) and non preferred (waterbuck) hosts. J Chem Ecol 29:2331–2345
Gomez LE, Coen CE (2013) Insect attractant formulations and insect control. US Patent no. WO2013173300 A1
Haddi K, Berger M, Bielza P, Cifuentes D, Field LM, Gorman K, Rapisarda C, Williamson MS, Bass C (2012) Identification of mutations associated with pyrethroid resistance in the voltage-gated sodium channel of the tomato leaf miner (Tuta absoluta). Insect Biochem Mol Biol 42:506–513
Hausen BM, Reichling J, Harkenthal M (1999) Degradation products of monoterpenes are the sensitizing agents in tea tree oil. Am J Contact Derm 10:68–77
Huang Y, Shuit-Hung HOSH, Lee HC, Yap YL (2002) Insecticidal properties of eugenol, isoeugenol and methyleugenol and their effects on nutrition of Sitophilus zeamais Motsch. (Coleoptera: Curculionidae) and Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae). J Stored Prod Res 38:403–412
Hussain AI, Anwar F, Sherazi STH, Przybylski R (2007) Chemical composition, antioxidant and antimicrobial activities of basil (Ocimum basilicum) essential oils depends on seasonal variations. Food Chem 108:986–995
Isman MB (2006) Botanical insecticides, deterrents, and repellents in modern agriculture and an increasingly regulated world. Annu Rev Entomol 51:45–66
Isman MB (2019) Commercial development of plant essential oils and their constituents as active ingredients in bioinsecticides. Phytochem Rev 19:235–241. https://doi.org/10.1007/s11101-019-09653-9
Isman MB, Wilson JA, Bradbury R (2008) Insecticidal activities of commercial rosemary oils (Rosmarinus officinalis) against larvae of Pseudaletia unipuncta and Trichoplusia ni in relation to their chemical compositions. Pharm Biol 46:82–87. https://doi.org/10.1080/13880200701734661
Junnila A, Revay EE, Müller GC, Kravchenko V, Qualls WA, Xue d R, Allen SA, Beier JC, Schlein Y (2015) Efficacy of attractive toxic sugar baits (ATSB) against Aedes albopictus with garlic oil encapsulated in β-cyclodextrin as the active ingredient. Acta Trop 152:195–200
Kéita SM, Vincent C, Schmit JP, Bélanger A (2001) Essential oil composition of Ocimum basilicum L., O. Gratissimum L. and O. Suave L. in the Republic of Guinea. Flavour Frag J 15:339–341
Khani A, Asghari J (2012) Insecticide activity of essential oils of Mentha longifolia, Pulicaria gnaphalodes and Achillea wilhelmsii against two stored product pests, the flour beetle, Tribolium castaneum, and the cowpea weevil, Callosobruchus maculatus. J Insect Sci 12:73–10. https://doi.org/10.1673/031.012.7301
Khiyari MEA, Kasrati A, Jamali CA, Zeroual S, Markouk M, Bekkouche K, Wohlmuth H, Leach D, Abbad A (2014) Chemical composition, antioxidant and insecticidal properties of essential oils from wild and cultivated Salvia aucheri subsp. blancoana (Webb. & Helder), an endemic, threatened medicinal plant in Morocco. Ind Crop Prod 57:106–109
Khoshtinat K, Barzegar M, Sahari MA, Hamidi Z (2017) Encapsulation of Iranian garlic oil with β-cyclodextrin: optimization and its characterization. J Agr Sci Tech-Iran 19:97–111
Kleinbaum DG, Klein M (2012) Survival analysis - a self-learning text, 3rd edn. Springer Publishers, New York
Klocke JA, Darlington MV, Balandrin MF (1987) 1,8-Cineole (eucalyptol), a mosquito feeding and ovipositional repellent from volatile oil of Hemizonia fitchii (Asteraceae). J Chem Ecol 13:2131–2141
Korycinska A, Moran H (2009) Plant pest notice: South American tomato moth, Tuta absoluta (No. 56), pp1–4, Department for Environment. Food and Rural Affairs, Food Environment Research Agency
Lawal OA, Ogunwande IA, Omikorede OE, Owolabi MS, Olorunsola FF, Sanni AAO, Amisu KO, Opoku AR (2014) Chemical composition and antimicrobial activity of essential oil of Ocimum kilimandscharicum (R. Br.) Guerke: a new chemotype. Am J Essent Oil Nat Prod 2:41–46
Lee SE, Lee BH, Choi WS, Park BS, Kim JG, Campbell BC (2001) Fumigant toxicity of volatile natural products from Korean spices and medicinal plants towards the rice weevil, Sitophilus oryzae (L). Pest Manag Sci 57:548–553
Lee EJ, Kim JR, Choi DR, Ahn YJ (2008) Toxicity of cassia and cinnamon oil compounds and cinnamaldehyde-related compounds to Sitophilus oryzae (Coleoptera: Curculionidae). J Econ Entomol 101:1960–1966
Lietti MMM, Botto E, Alzogaray RA (2005) Insecticide resistance in Argentine populations of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Neotropical Entomol 34:113–119
Lima AS, Milhomem MN, Monteiro OS, Arruda ACP, de Castro JAM, Fernandes YML, Maia JGS, Costa-Junior LM (2018) Seasonal analysis and acaricidal activity of the thymol-type essential oil of Ocimum gratissimum and its major constituents against Rhipicephalus microplus (Acari: Ixodidae). Parasitol Res 117:59–65
Marques HMC (2010) A review on cyclodextrin encapsulation of essential oils and volatiles. Flavour Frag J 25:313–326
Matasyoh LG, Matasyoh JC, Wachira FN, Kinyua MG, Muigai AWT, Mukiama TK (2007) Chemical composition and antimicrobial activity of the essential oil of Ocimum gratissimum L. growing in eastern Kenya. Afr J Biotechnol 6:760–765
Mazyad SA, Soliman M (2001) Laboratory evaluation of the insecticidal activity of camphor on the development of Oestrus ovis larvae. J Egypt Soc Parasitol 31:887–892
McDonald LL, Guy RH, Speirs RD (1970) Preliminary evaluation of new candidate materials as toxicants, repellents and attractants against stored product insects. Marketing Research Report No. 882, Agriculture Research Service, US Department of Agriculture, Washington
Mossa ATH, Abdelfattahn NAH, Mohafrash SMM (2017) Nanoemulsion of camphor (Eucalyptus globulus) essential oil, formulation, characterization and insecticidal activity against wheat weevil, Sitophilus granarius. Asian J Crop Sci 9:50–62. https://doi.org/10.3923/ajcs.2017.50.62
Ngoh SP, Choo-LEW PFY, Huang Y, Kini MR, Ho SH (1998) Insecticidal and repellent properties of nine volatile constituents of essential oils against the American cockroach, Periplaneta americana (L.). Pestic Sci 54:261–268
Nguemtchouin MG, Ngassoum MB, Chalier P, Kamga R, Ngamo LS, Cretin M (2013) Ocimum gratissimum essential oil and modified montmorillonite clay, a means of controlling insect pests in stored products. J Stored Prod Res 52:57–62
NIST (2008) NIST Standard Reference Database, National Institutes of Standards and Technology, NIST/EPA/NIH Mass Spectral Library. http://www.nist.gov
Ntezurubanza L, Scheffer JJC, Looman A, Baerheim AS (1984) Composition of essential oil of Ocimum kilimandscharicum grown in Rwanda. Planta Med 50:385–388
Ntonga PA, Baldovini N, Mouray E, Mambu L, Belong P, Grellier P (2014) Activity of Ocimum basilicum, Ocimum canum, and Cymbopogon citratus essential oils against Plasmodium falciparum and mature-stage larvae of Anopheles funestus s.s. Parasite 21:33. https://doi.org/10.1051/parasite/2014033
Ogendo JO, Kostyukovsky M, Ravid U, Matasyoh JC, Deng AL, Omolo EO, Kariuki ST, Shaaya E (2008) Bioactivity of Ocimum gratissimum L. oil and two of its constituents against five insect pests attacking stored food products. J Stored Prod Res 44:328–334
Ojimelukwe PC, Adler C (2000) Toxicity and repellent effects of eugenol, thymol, linalool, menthol and other pure compounds on Dinoderus bifloveatus (Coleoptera: Bostrichidae). J Sustain Agr 2:47–54
Padalia RC, Verma RS, Chauhan A (2014) Analyses of organ specific variations in essential oils of four Ocimum species. J Essent Oil Res 26:409–419. https://doi.org/10.1080/10412905.2014.942808
Pavela R, Sedlak P (2018) Post-application as a factor influencing the insecticidal activity of essential oil from Thymus vulgaris. Ind Crops Prod 113:46–49. https://doi.org/10.1016/j.indcrop.2018.01.021
Pavela R, Maggi F, Petrelli R, Cappellacci L, Buccioni M, Palmieri A, Canale A, Benelli G (2020) Outstanding insecticidal activity and sublethal effects of Carlina acaulis root essential oil on the housefly, Musca domestica, with insights on its toxicity on human cells. Food Chem Toxicol 136:111037. https://doi.org/10.1016/j.fct.2019.111037
Pavoni L, Perinelli DR, Bonacucina G, Cespi M, Palmieri GF (2020) An overview of micro- and nanoemulsions as vehicles for essential oils: formulation, preparation and stability. Nanomaterials 10(135):1–24. https://doi.org/10.3390/nano10010135
R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Ram SV, Rajendra CP, Amit C, Sanjog TT (2013) Exploring compositional diversity in the essential oils of 34 Ocimum taxa from Indian flora. Ind Crop Prod 45:7–19
Roditakis E, Vasakis E, Grispou M, Stavrakaki M, Nauen R, Gravouil M, Bassi A (2015) First report of Tuta absoluta resistance to diamide insecticides. J Pest Sci 88:9–16
Ryan MF, Bryan O (1988) Plant-insect coevolution and inhibition of acetylcholinesterase. J Chem Ecol 14:1965–1975
Said-Al Ahl H, Hikal WM, Tkachenko KG (2017) Essential oils with potential as insecticidal agents: a review. J Environ Plann Man 3:23–33
Sarin RV, Narwal S, Bafna PA (2013) Anti-diarrhoeal activity of aqueous extract of Ocimum kilimandscharicum. J Ethnopharmacol 148:223–228
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
Soliman EA, Yel-M A, Smel-D M, Magdy AM (2013) Microencapsulation of essential oils within alginate: formulation and in vitro evaluation of antifungal activity. J Encapsul Adsorp Sci 3:48–55
Sylla S, Brévault T, Bal AB, Chailleux A, Diatte M, Desneux N, Diarra K (2017) Rapid spread of the tomato leafminer, Tuta absoluta (Lepidoptera : Gelechiidae), an invasive pest in sub-Saharan Africa. Entomol Gen 36:269–283
Umerie SC, Anaso HU, Anyasoro LJC (1998) Insecticidal potentials of Ocimum basilicum leaf-extract. Bioresour Technol 64:237–239
Vieira RF, Grayer RJ, Paton A, Simon JE (2001) Genetic diversity of Ocimum gratissimum L. based on volatile oil constituents, flavonoids and RAPD markers. Biochem Syst Ecol 29:287–304
WHO (1996) Report of the WHO Informal Consultation on the Evaluation and Testing of Insecticides. WHO/HQ, Geneva, 7 to 11 October. : 32–36; 50–52. https://apps.who.int/iris/handle/10665/65962
Xian X (2017) The potential invasion risk of the tomato leafminer Tuta absoluta in China. In Conference. Ottawa, Canada, 30th August 2017, 1–37
Yarou BB, Bawin T, Boullis A, Heukin S, Lognay G, Verheggen FJ, Francis F (2017) Oviposition deterrent activity of basil plants and their essentials oils against Tuta Absoluta (Lepidoptera: Gelechiidae). Environ Sci Pollut Res Int 25:29880–29888
Zhu J, Zeng X, O’neal M, Schultz G, Tucker B, Coats J, Bartholomay L, Xue RD (2008) Mosquito larvicidal activity of botanical-based mosquito repellents. J Am Mosquito Contr 24:161–168. https://doi.org/10.2987/8756-971X(2008)24[161:MLAOBM]2.0.CO;2
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We gratefully acknowledge the financial support for the German Academic Exchange Service In-Region scholarship for funding FREE. SAM thanks the Federal Ministry of Cooperation and Development (BMZ), Germany for providing the financial support through ICIPE Tuta absoluta IPM project.
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Essoung, F.R.E., Tadjong, A.T., Chhabra, S.C. et al. Repellence and fumigant toxicity of essential oils of Ocimum gratissimum and Ocimum kilimandscharicum on Tuta absoluta (Lepidoptera: Gelechiidae). Environ Sci Pollut Res 27, 37963–37976 (2020). https://doi.org/10.1007/s11356-020-09773-2
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DOI: https://doi.org/10.1007/s11356-020-09773-2