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Toxic effects of two essential oils and their constituents on the mealworm beetle, Tenebrio molitor

Published online by Cambridge University Press:  14 December 2017

L.C. Martínez*
Affiliation:
Departamento de Entomologia, Universidade Federal de Viçosa, 36570-000, Viçosa, Minas Gerais, Brasil
A. Plata-Rueda
Affiliation:
Instituto de Ciências Agrárias, Universidade Federal de Viçosa, 38810-000, Viçosa, Minas Gerais, Brasil
H.C. Colares
Affiliation:
Departamento de Fitotecnia, Universidade Federal de Viçosa, 36570-000, Viçosa, Minas Gerais, Brasil
J.M. Campos
Affiliation:
Departamento de Fitotecnia, Universidade Federal de Viçosa, 36570-000, Viçosa, Minas Gerais, Brasil
M.H. Dos Santos
Affiliation:
Departamento de Química, Universidade Federal de Viçosa, 36570-000, Viçosa, Minas Gerais, Brasil
F.L. Fernandes
Affiliation:
Instituto de Ciências Agrárias, Universidade Federal de Viçosa, 38810-000, Viçosa, Minas Gerais, Brasil
J.E. Serrão
Affiliation:
Departamento de Biologia Geral, Universidade Federal de Viçosa, 36570-000, Viçosa, Minas Gerais, Brasil
J.C. Zanuncio
Affiliation:
Departamento de Entomologia, Universidade Federal de Viçosa, 36570-000, Viçosa, Minas Gerais, Brasil
*
*Author for correspondence Phone: +55 31 3899-4012 Fax: +55 31 3899-2108 E-mail: [email protected]

Abstract

The study identified insecticidal effects from the cinnamon and clove essential oils in Tenebrio molitor L. (Coleoptera: Tenebrionidae). The lethal concentrations (LC50 and LC90), lethal time, and repellent effect on larvae, pupae, and adults of T. molitor after exposure to six concentrations of each essential oil and toxic compounds were evaluated. The chemical composition of the cinnamon oil was also determined and primary compounds were eugenol (10.19%), trans-3-caren-2-ol (9.92%), benzyl benzoate (9.68%), caryophyllene (9.05%), eugenyl acetate (7.47%), α-phellandrene (7.18%), and α-pinene (6.92%). In clove essential oil, the primary compounds were eugenol (26.64%), caryophyllene (23.73%), caryophyllene oxide (17.74%), 2-propenoic acid (11.84%), α-humulene (10.48%), γ-cadinene (4.85%), and humulene oxide (4.69%). Cinnamon and clove essential oils were toxic to T. molitor. In toxic chemical compounds, eugenol have stronger contact toxicity in larvae, pupae, and adult than caryophyllene oxide, followed by α-pinene, α-phellandrene, and α-humulene. In general, the two essential oils were toxic and repellent to adult T. molitor. Cinnamon and clove essential oils and their compounds caused higher mortality and repellency on T. molitor and, therefore, have the potential for integrated management programs of this insect.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2017 

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References

Arthur, F.H. (1996) Grain protectants: current status and prospects for the future. Journal of Stored Products Research 32, 293302.Google Scholar
Bakkali, F., Averbeck, S. & Averbeck, D. (2008) Biological effects of essential oils – a review. Food and Chemical Toxicology 46, 446475.Google Scholar
Banthorpe, D.V., Charlwood, B.V. & Francis, M.J.O. (1972) Biosynthesis of monoterpenes. Chemical Reviews 72, 115155.Google Scholar
Barnes, A.I. & Siva-Jothy, M.T. (2000) Density-dependent prophylaxis in the mealworm beetle Tenebrio molitor L. (Coleoptera: Tenebrionidae): cuticular melanization is an indicator of investment in immunity. Proceedings of the Royal Society of London B 267, 177182.Google Scholar
Candy, D.J. (1978) The regulation of locust flight muscle metabolism by octopamine and other compounds. Insect Biochemistry 8, 177181.Google Scholar
Chaieb, K., Hajlaoui, H., Zmantar, T., Kahla-Nakbi, A.B., Rouabhia, M., Mahdouani, K. & Bakhrouf, A. (2007) The chemical composition and biological activity of clove essential oil, Eugenia caryophyllata (Syzigium aromaticum L. Myrtaceae): a short review. Phytotherapy Research 21, 501506.Google Scholar
Chermenskaya, T.D., Stepanycheva, E.A., Shchenikova, A.V. & Chakaeva, A.S. (2010) Insecto acaricidal and deterrent activities of extracts of Kyrgyzstan plants against three agricultural pests. Industrial Crops and Products 32, 157163.Google Scholar
Choi, W.I., Lee, E.H., Choi, B.R., Park, H.M. & Ahn, Y.J. (2003) Toxicity of plant essential oils to Trialeurodes vaporariorum (Homoptera: Aleyrodidae). Journal of Economic Entomology 96, 14791484.Google Scholar
Correa, Y.D.C.G., Faroni, L.R., Haddi, K., Oliveira, E.E. & Pereira, E.J.G. (2015) Locomotory and physiological responses induced by clove and cinnamon essential oils in the maize weevil Sitophilus zeamais. Pesticide Biochemistry and Physiology 125, 3137.Google Scholar
Cosimi, S., Rossi, E., Cioni, P. & Canale, A. (2009) Bioactivity and qualitative analysis of some essential oils from Mediterranean plants against stored-products pest: evaluation of repellency against Sitophilus zeamais Motschulsky, Cryptolestes ferrugineus (Stephens) and Tenebrio molitor (L.). Journal of Stored Products Research 45, 125132.Google Scholar
Dapkevicius, A., Venskutonis, R., Van Beek, T.A. & Linssen, J.P.H. (1998) Antioxidant activity of extracts obtained by different isolation procedures from some aromatic herbs grown in Lithuania. Journal of the Science and Food Agriculture 77, 140146.Google Scholar
Dunkel, F.V. (1992) The stored grain ecosystem: a global perspective. Journal of Stored Products Research 28, 7387.Google Scholar
Enan, E. (2001) Insecticidal activity of essential oils: octopaminergic sites of action. Comparative Biochemistry and Physiology Part C: Toxicology and Pharmacology 130, 325337.Google Scholar
Farooqui, T. (2007) Octopamine-mediated neuromodulation of insect senses. Neurochemical Research 32, 15111529.Google Scholar
Fazolin, M., Estrela, J., Catani, V., Alécio, M. & Lima, M. (2007) Propriedade inseticida dos óleos essenciais de Piper hispidinervum C. DC.; Piper aduncum L. e Tanaecium nocturnum (Barb. Rodr.) Bur. & K. Shum sobre Tenebrio molitor L. 1758. Ciência e Agrotecnologia 31, 113120.Google Scholar
Fichi, G., Flamini, G., Zaralli, L.J. & Perrucci, S. (2007) Efficacy of an essential oil of Cinnamomum zeylanicum against Psoroptes cuniculi. Phytomedicine 14, 227231.Google Scholar
Finney, D.J. (1964) Probit Analysis. Cambridge, UK, Cambridge University Press.Google Scholar
Flinn, P.W., Hagstrum, D.W., Reed, C. & Phillips, T.W. (2003) United States department of agriculture-agricultural research service stored-grain area-wide integrated pest management program. Pest Management Science 59, 614618.Google Scholar
Goni, P., Lopez, P., Sánchez, C., Gómez-Lus, R., Becerril, R. & Nerín, C. (2009) Antimicrobial activity in the vapour phase of a combination of cinnamon and clove essential oils. Food Chemistry 116, 982989.Google Scholar
Gunasena, G.H., Vinson, S.B., Williams, H.J. & Stipanovic, R.D. (1988) Effects of caryophyllene, caryophyllene oxide, and their interaction with gossypol on the growth and development of Heliothis virescens (F.) (Lepidoptera: Noctuidae). Journal of Economic Entomology 81, 9397.Google Scholar
Haddi, K., Oliveira, E.E., Faroni, L.R., Guedes, D.C. & Miranda, N.N. (2015) Sublethal exposure to clove and cinnamon essential oils induces hormetic-like responses and disturbs behavioral and respiratory responses in Sitophilus zeamais (Coleoptera: Curculionidae). Journal of Economic Entomology 108, 28152822.Google Scholar
Ho, S.H., Cheng, L.P.L., Sim, K.Y. & Tan, H.T.W. (1994) Potential of cloves (Syzygium aromaticum) (L.) Merr. and Perry as a grain protectant against Tribolium castaneum (Herbst) and Sitophilus zeamais Motsch. Postharvest Biology and Technology 4, 179183.Google Scholar
Huang, Y., Ho, S.H., Lee, H.C. & Yap, Y.L. (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). Journal of Stored Products Research 38, 403412.Google Scholar
Isman, M.B. (2000) Plant essential oils for pest and disease management. Crop Protection 19, 603608.Google Scholar
Isman, M.B. (2006) Botanical insecticides, deterrents, and repellents in modern agriculture and an increasingly regulated world. Annual Review of Entomology 51, 4566.Google Scholar
Jemâa, J.M.B., Tersim, N., Toudert, K.T. & Khouja, M.L. (2012) Insecticidal activities of essential oils from leaves of Laurus nobilis L. from Tunisia, Algeria and Morocco, and comparative chemical composition. Journal of Stored Products Research 48, 97104.Google Scholar
Jirovetz, L., Buchbauer, G., Stoilova, I., Stoyanova, A., Krastanov, A. & Schmidt, E. (2006) Chemical composition and antioxidant properties of clove leaf essential oil. Journal of Agricultural and Food Chemistry 54, 63036307.Google Scholar
Jumbo, L.O.V., Faroni, L.R., Oliveira, E.E., Pimentel, M.A. & Silva, G.N. (2014) Potential use of clove and cinnamon essential oils to control the bean weevil, Acanthoscelides obtectus Say, in small storage units. Industrial Crops and Products 56, 2734.Google Scholar
Kim, S.I., Roh, J.Y., Kim, D.H., Lee, H.S. & Ahn, Y.J. (2003) Insecticidal activities of aromatic plant extracts and essential oils against Sitophilus oryzae and Callosobruchus chinensis. Journal of Stored Products Research 39, 293303.Google Scholar
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, 11011106.Google Scholar
Lee, E.J., Kim, J.R., Choi, D.R. & Ahn, Y.J. (2008) Toxicity of cassia and cinnamon oil compounds and cinnamaldehyde-related compounds to Sitophilus oryzae (Coleoptera: Curculionidae). Journal of Economic Entomology 101, 19601966.Google Scholar
Lerdau, M., Litvak, M. & Monson, R. (1994) Plant chemical defense: monoterpenes and the growth-differentiation balance hypothesis. Trends in Ecology & Evolution 9, 5861.Google Scholar
Livingstone, M., Harria-Warrick, R. & Kravitz, E.A. (1980) Serotonin and octopamine produce opposite postures in lobsters. Science 208, 7679.Google Scholar
Loudon, C. (1988) Development of Tenebrio molitor in low oxygen levels. Journal of Insect Physiology 34, 97103.Google Scholar
Loza-Tavera, H. (1999) Monoterpenes in essential oils. Advances in Experimental Medicine and Biology 464, 4962.Google Scholar
Martínez, L.C., Plata-Rueda, A., Zanuncio, J.C. & Serrão, J.E. (2015) Bioactivity of six plant extracts on adults of Demotispa neivai (Coleoptera: Chrysomelidae). Journal of Insect Science 15(34), 15.Google Scholar
Neethirajan, S., Karunakaran, C., Jayas, D.S. & White, N.D.G. (2007) Detection techniques for stored-product insects in grain. Food Control 18, 157162.Google Scholar
Orchard, I. (1982) Octopamine in insects: neurotransmitter, neurohormone, and neuromodulator. Canadian Journal of Zoology 60, 659669.Google Scholar
Padin, S., Ringuelet, J.A., Bello, D., Cerimele, E.L., Re, M.S. & Henning, C.P. (2000) Toxicology and repellent activity of essential oils on Sitophilus oryzae L. and Tribolium castaneum Herbst. Journal of Herbs, Spices and Medicinal Plants 7, 6773.Google Scholar
Park, I.K., Lee, S.G., Choi, D.H., Park, J.D. & Ahn, Y.J. (2003) Insecticidal activities of constituents identified in the essential oil from leaves of Chamaecyparis obtusa against Callosobruchus chinensis (L.) and Sitophilus oryzae (L.). Journal of Stored Products Research 39, 375384.Google Scholar
Plata-Rueda, A., Martínez, L.C., Dos Santos, M.H., Fernandes, F.L., Wilcken, C.F., Soares, M.A., Serrão, J.E. & Zanuncio, J.C. (2017) Insecticidal activity of garlic essential oil and their constituents against the mealworm beetle, Tenebrio molitor Linnaeus (Coleoptera: Tenebrionidae). Scientific Reports 7, 46406.Google Scholar
Punzo, F. & Mutchmor, J.A. (1980) Effects of temperature, relative humidity and period of exposure on the survival capacity of Tenebrio molitor (Coleoptera: Tenebrionidae). Journal of the Kansas of Entomological Society 53, 260270.Google Scholar
Regnault-Roger, C., Hamraoui, A., Holeman, M., Theron, E. & Pinel, R. (1993) Insecticidal effect of essential oils from Mediterranean plants upon Acanthoscelides obtectus Say (Coleoptera, Bruchidae), a pest of kidney bean (Phaseolus vulgaris L.). Journal of Chemical Ecology 19, 12331244.Google Scholar
SAS Institute. (2002) The SAS System for Windows, Release 9.0. Cary, NC, SAS Institute.Google Scholar
Schroeckenstein, D.C., Meier-Davis, S. & Bush, R.K. (1990) Occupational sensitivity to Tenebrio molitor Linnaeus (yellow mealworm). Journal of Allergy and Clinical Immunology 86, 182188.Google Scholar
Shaaya, E., Kostjukovski, M., Eilberg, J. & Sukprakarn, C. (1997) Plant oils as fumigants and contact insecticides for the control of stored-product insects. Journal of Stored Products Research 33, 715.Google Scholar
Shahverdi, A.R., Monsef-Esfahani, H.R., Tavasoli, F., Zaheri, A. & Mirjani, R. (2007) Trans-cinnamaldehyde from Cinnamomum zeylanicum bark essential oil reduces the clindamycin resistance of Clostridium difficile in vitro. Journal of Food Science 72, S55S58.Google Scholar
Simić, A., Soković, M.D., Ristić, M., Grujić-Jovanović, S., Vukojević, J. & Marin, P.D. (2004) The chemical composition of some Lauraceae essential oils and their antifungal activities. Phytotherapy Research 18, 713717.Google Scholar
Stefanazzi, N., Stadler, T. & Ferrero, A. (2011) Composition and toxic, repellent and feeding deterrent activity of essential oils against the stored-grain pests Tribolium castaneum (Coleoptera: Tenebrionidae) and Sitophilus oryzae (Coleoptera: Curculionidae). Pest Management Science 67, 639646.Google Scholar
Wasserthal, L.T. (1996) Interaction of circulation and tracheal ventilation in holometabolous insects. Advances of Insect Physiology 26, 297351.Google Scholar
Whim, M.D. & Evans, P.D. (1988) Octopaminergic modulation of flight muscle in the locust. Journal of Experimental Biology 134, 247266.Google Scholar
XLSTAT. (2004) XLSTAT for Excel. Addinsoft, UK.Google Scholar
Yang, Y.C., Lee, H.S., Lee, S.H., Clark, J.M. & Ahn, Y.J. (2005) Ovicidal and adulticidal activities of Cinnamomum zeylanicum bark essential oil compounds and related compounds against Pediculus humanus capitis (Anoplura: Pediculicidae). International Journal of Parasitology 35, 15951600.Google Scholar
Yoo, C.B., Han, K.T., Cho, K.S., Ha, J., Park, H.J., Nam, J.H. & Lee, K.T. (2005) Eugenol isolated from the essential oil of Eugenia caryophyllata induces a reactive oxygen species-mediated apoptosis in HL-60 human promyelocytic leukemia cells. Cancer Letters 225, 4152.Google Scholar
Zanuncio, J.C., Mourão, S.A., Martínez, L.C., Wilcken, C.F., Ramalho, F.S., Plata-Rueda, A. & Serrão, J.E. (2016) Toxic effects of the neem oil (Azadirachta indica) formulation on the stink bug predator, Podisus nigrispinus (Heteroptera: Pentatomidae). Scientific Reports 6, 30261.Google Scholar
Zapata, N. & Smagghe, G. (2010) Repellency and toxicity of essential oils from the leaves and bark of Laurelia sempervirens and Drimys winteri against Tribolium castaneum. Industrial Crops and Products 32, 405410.Google Scholar
Zettler, J.L. & Arthur, F.H. (2000) Chemical control of stored product insects with fumigants and residual treatments. Crop Protection 19, 577582.Google Scholar