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Bioactivity of some Apiaceae essential oils and their constituents against Sitophilus zeamais (Coleoptera: Curculionidae)

Published online by Cambridge University Press:  09 December 2019

J. S. Rosa ,
L. Oliveira Open the ORCID record for L. Oliveira [Opens in a new window] ,
R. M. O. F. Sousa ,
C. B. Escobar  and
M. Fernandes-Ferreira
J. S. Rosa
Affiliation:
Universidade dos Açores, Faculdade de Ciências e Tecnologias, Centro de Biotecnologia dos Açores, Rua da Mãe de Deus, 9501-801 Ponta Delgada, S. Miguel, Açores, Portugal
L. Oliveira*
Affiliation:
Universidade dos Açores, Faculdade de Ciências e Tecnologias, Centro de Biotecnologia dos Açores, Rua da Mãe de Deus, 9501-801 Ponta Delgada, S. Miguel, Açores, Portugal
R. M. O. F. Sousa
Affiliation:
Department of Biology, Faculty of Science, University of Porto, Rua do Campo Alegre s/n, 4169-007Porto, Portugal GreenUPorto – Sustainable Agrifood Production Research Centre, Campus de Vairão, Rua da Agrária 747, 4485-646Vila do Conde, Portugal CITAB, Centre for the Research and Technology of Agro-Environmental and Biological Sciences. UTAD, Universidade de Trás-os-Montes e Alto Douro, Quinta de Prados, 5001-801Vila Real, Portugal
C. B. Escobar
Affiliation:
Universidade dos Açores, Faculdade de Ciências e Tecnologias, Centro de Biotecnologia dos Açores, Rua da Mãe de Deus, 9501-801 Ponta Delgada, S. Miguel, Açores, Portugal
M. Fernandes-Ferreira
Affiliation:
Department of Biology, Faculty of Science, University of Porto, Rua do Campo Alegre s/n, 4169-007Porto, Portugal GreenUPorto – Sustainable Agrifood Production Research Centre, Campus de Vairão, Rua da Agrária 747, 4485-646Vila do Conde, Portugal CITAB, Centre for the Research and Technology of Agro-Environmental and Biological Sciences. UTAD, Universidade de Trás-os-Montes e Alto Douro, Quinta de Prados, 5001-801Vila Real, Portugal MAPPROD Lda, Rua António de Mariz, 22, 4715-279Braga, Portugal
*
Author for correspondence: L. Oliveira, E-mail: [email protected]
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Abstract

Sitophilus zeamais is a key pest of stored grains. Its control is made, usually, using synthetic insecticides, despite their negative impacts. Botanical insecticides with fumigant/repellent properties may offer an alternative solution. This work describes the effects of Anethum graveolens, Petroselinum crispum, Foeniculum vulgare and Cuminum cyminum essential oils (EOs) and (S)-carvone, cuminaldehyde, estragole and (+)-fenchone towards adults of S. zeamais. Acute toxicity was assessed by fumigation and topical application. Repellence was evaluated by an area preference bioassay and two-choice test, using maize grains. LC50 determined by fumigation ranged from 51.8 to 535.8 mg L−1 air, with (S)-carvone being the most active. LD50 values for topical applications varied from 23 to 128 µg per adult for (S)-carvone > cuminaldehyde > A. graveolens > C. cyminum > P. crispum. All EOs/standard compounds reduced significantly the percentage of insects attracted to maize grains (65–80%) in the two-choice repellence test, whereas in the area preference bioassay RD50 varied from 1.4 to 45.2 µg cm−2, with cuminaldehyde, (S)-carvone and estragole being strongly repellents. Petroselinum crispum EO and cuminaldehyde affected the nutritional parameters relative growth rate, efficiency conversion index of ingested food and antifeeding effect, displaying antinutritional effects toward S. zeamais. In addition, P. crispum and C. cyminum EOs, as well as cuminaldehyde, showed the highest acetylcholinesterase inhibitory activity in vitro (IC50 = 185, 235 and 214.5 µg mL−1, respectively). EOs/standard compounds exhibited acute toxicity, and some treatments showed antinutritional effects towards S. zeamais. Therefore, the tested plant products might be good candidates to be considered to prevent damages caused by this pest.

Keywords

Acetylcholinesterase inhibitionApiaceaemaize weevilsnutritional effectsrepellence
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 110 , Issue 3 , June 2020 , pp. 406 - 416
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Copyright
Copyright © Cambridge University Press 2019

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References

Aazza, S, Lyoussi, B and Miguel, MG (2011) Antioxidant and antiacetylcholinesterase activities of some commercial essential oils and their major compounds. Molecules 16, 7672–7690. https://doi:10.3390/molecules16097672.CrossRefGoogle ScholarPubMed
Abdelgaleil, SAM, Mohamed, MIE, Badawy, MEI and El-Arami, SAA (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, 518–525. https://doi:10.1007/s10886-009-9635-3.CrossRefGoogle ScholarPubMed
Arruda, M, Viana, H, Rainha, N, Neng, NR, Rosa, JS, Nogueira, JMF and Barreto, MC (2012) Anti-acetylcholinesterase and antioxidant activity of essential oils from Hedychium gardnerianum Sheppard ex Ker-Gawl. Molecules 17, 3082–3092. https://doi:10.3390/molecules17033082.CrossRefGoogle Scholar
Askar, SI, Al-Assal, MS and Nassar, AMK (2016) Efficiency of some essential oils and insecticides in the control of some Sitophilus insects (Coleoptera: Curculionidae). Egyptian Journal of Plant Protection. Research 4, 39–55.Google Scholar
Athanassiou, CG, Kavallieratos, NG and Campbell, JF (2017) Competition of three species of Sitophilus on rice and maize. PLoS One 12, e0173377. https://doi:10.1371/journal.pone.0173377.CrossRefGoogle ScholarPubMed
Bedini, S, Bougherra, HH, Flamini, G, Cosci, F, Belhamel, K, Ascrizzi, R and Conti, B (2016) Repellency of anethole- and estragole-type fennel essential oils against stored prain pest: the different twins. Bulletin of Insectology 69, 149–157.Google Scholar
Benzi, V, Stefanazzi, N and Ferrero, AA (2009) Biological activity of essential oils from leaves and fruits of pepper tree (Schinus molle L.) to control rice weevil (Sitophilus oryzae L.). Chilean Journal of Agricultural Research 69, 154–159. http://dx.doi.org/10.4067/S0718-58392009000200004.CrossRefGoogle Scholar
Bertoli, A, Conti, B, Mazzoni, V, Meini, L and Pistelli, L (2012) Volatile chemical composition and bioactivity of six essential oils against the stored food insect Sitophilus zeamais Motsch. (Coleoptera Dryophthoridae). Natural Product Research 26, 2063–2071. https://doi:10.1080/14786419.2011.607453.Google Scholar
Bonesi, M, Menichini, F, Tundis, R, Loizzo, MR, Conforti, F, Passalacqua, NG, Statti, GA and Menichini, F (2010) Acetylcholinesterase and butyrylcholinesterase inhibitory activity of Pinus species essential oils and their constituents. Journal of Enzyme Inhibition and Medicinal Chemistry 25, 622–628. https://doi:10.3109/14756360903389856.CrossRefGoogle ScholarPubMed
Boulogne, I, Petit, P, Ozier-Lafontaine, H, Desfontaines, L and Loranger-Merciris, G (2012) Insecticidal and antifungal chemicals produced by plants: a review. Environmental Chemistry Letters 10, 325–347.CrossRefGoogle Scholar
Camaroti, JRSL, de Almeida, WA, do Rego Belmonte, B, de Oliveira, APS, de Albuquerque Lima, T, Ferreira, MRA, Paiva, PMG, Soares, LAL, Pontual, EV and Napoleão, TH (2018) Sitophilus zeamais adults have survival and nutrition affected by Schinus terebinthifolius leaf extract and its lectin (SteLL). Industrial Crops and Products 116, 81–89. https://doi.org/10.1016/j.indcrop.2018.02.065.CrossRefGoogle Scholar
Chaubey, MK (2008) Fumigant toxicity of essential oils from some common spices against pulse beetle, Callosobruchus chinensis (Coleoptera: Bruchidae). Journal of Oleo Science 57, 171–179. https://doi.org/10.5650/jos.57.171.CrossRefGoogle Scholar
Chaubey, MK (2011) Fumigant toxicity of essential oils against rice weevil Sitophilus oryzae L. (Coleoptera: Curculionidae). Journal of Biological Sciences 11, 411–416. https://doi:10.3923/jbs.2011.411.416.Google Scholar
Coats, JR, Karr, LL and Drewes, CD (1991) Toxicity and neurotoxic effects of monoterpenoids in insects and earthworms. In Heden, PA (ed.), Naturally Occurring Pest Bioregulators. ACS Symposium Series 449, American Chemical Society, Washington, DC, pp. 305–316. doi: 10.1021/bk-1991-0449.ch020.CrossRefGoogle Scholar
Colares, T, Dionello, RG and Radunz, LL (2016) Susceptibility of different genotypes of rice to Sitophilus zeamais Motschulsky 1885 attack (Coleoptera: Curculionidae). Revista Brasileira de Engenharia Agrícola e Ambiental 20, 275–279. http://dx.doi.org/10.1590/18071929/agriambi.v20n3p275-279.CrossRefGoogle Scholar
Cosimi, S, Rossi, E, Cioni, PL and Canale, A (2009) Bioactivity and qualitative analysis some essential oils from Mediterranean plants against stored-product pests: evaluation of repellency against Sitophilus zeamais Motschulsky, Cryptolestes ferrugineus (Stephens) and Tenebrio molitor (L.). Journal of Stored Products Research 45, 125–132. https://doi.org/10.1016/j.jspr.2008.10.002.CrossRefGoogle Scholar
de Lira, CS, Pontual, EV, de Albuquerque, LP, Paiva, LM, Paiva, PMG, de Oliveira, JV, Napoleão, TH and Navarro, DMDAF (2015) Evaluation of the toxicity of essential oil from Alpinia purpurata inflorescences to Sitophilus zeamais (maize weevil). Crop Protection 71, 95–100. https://doi.org/10.1016/j.cropro.2015.02.004.CrossRefGoogle Scholar
Ebadollahi, A (2011) Susceptibility of two Sitophilus species (Coleoptera: Curculionidade) to essential oils from Foeniculum vulgare and Satureja hortensis. Ecologia Balkanica 3, 1–8.Google Scholar
Ebadollahi, A (2013) Plant essential oils from Apiaceae family as alternatives to conventional insecticides. Ecologia Balkanica 5, 149–172.Google Scholar
Ebadollahi, A, Nouri-Ganbalani, G, Hoseini, SA and Sadeghi, GR (2012) Insecticidal activity of essential oils of five aromatic plants against Callosobruchus maculates F. (Coleoptera: Bruchidae) under laboratory conditions. Journal of Essential Oil Bearing Plants 15, 256–262. https://doi.org/10.1080/0972060X.2012.10644044.CrossRefGoogle Scholar
Ellman, GL, Courtney, KD, Valentino, A Jr and Feathertone, RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochemical Pharmacology 7, 88–95. https://doi.org/10.1016/0006-2952(61)90145-9.CrossRefGoogle ScholarPubMed
Evergetis, E, Michaelakis, A and Haroutounian, SA (2012) Essential oils of Umbelliferae (Apiaceae) family taxa as emerging potent agents for mosquito control. In Soloneski, S (ed.), Integrated Pest Management and Pest Control – Current and Future Tactics. IntechOpen Limited, London, UK, pp. 613–638. Available from: http://www.intechopen.com/books/integrated-pest-management-and-pestcontrol-current-and-future-tactics/essential-oils-of-umbelliferae-apiaceae-family-taxa-as-emerging-potentagents-for-mosquito-control. DOI: 10.5772/31777.Google Scholar
Evergetis, E, Michaelakis, A and Haroutounian, SA (2013) Exploitation of Apiaceae family essential oils as potent biopesticides and rich source of phellandrenes. Industrial Crops and Products 41, 365–370. https://doi.org/10.1016/j.indcrop.2012.04.058.CrossRefGoogle Scholar
Fang, R, Jiang, CH, Wang, XY, Zhang, HM, Liu, ZL, Zhou, L, Du, SS and Deng, ZW (2010) Insecticidal activity of essential oil of Carum carvi fruits from China and its main components against two grain storage insects. Molecules 15, 9391–9402. https://doi.org/10.3390/molecules15129391.CrossRefGoogle ScholarPubMed
França, SM, Oliveira, JV, Esteves Filho, AB and Oliveira, CM (2012) Toxicity and repellency of essential oils to Zabrotes subfasciatus (Boheman) (Coleoptera, Chrysomelidae, Bruchinae) in Phaseolus vulgaris L. Acta Amazonica 42, 381–386. http://dx.doi.org/10.1590/s0100-204x2017000100002.CrossRefGoogle Scholar
Huang, Y, Tan, JMWL, Kini, RM and Ho, SH (1997) Toxic and antifeedant action of nutmeg oil against Tribolium castaneum (Herbst) and Sitophilus zeamais Motsch. Journal of Stored Products Research 33, 289–298. https://doi.org/10.1016/S0022-474X(97)00009-X.CrossRefGoogle Scholar
Huang, Y, Lam, SL and Ho, SH (2000) Bioactivities of essential oil from Elletaria cardamomum (L.) Maton. to Sitophilus zeamais Motschulsky and Tribolium castaneum (Herbst). Journal of Stored Products Research 36, 107–117. https://doi:10.1016/S0022-474X(99)00040-5.CrossRefGoogle Scholar
Huang, Y, Ho, SH, Lee, HC and 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). Journal of Stored Products Research 38, 403–412.CrossRefGoogle Scholar
IBM (2015) IBM SPSS statistics for Windows, Version 23.0. IBM Corp, Armonk, NY.Google Scholar
Ingkanian, K, Temkitthawon, P, Chuenchom, K, Yuyaem, T and Thongnoi, W (2003) Screening for acetylcholinesterase inhibitory activity in plants used in Thai traditional rejuvenating and neurotonic remedies. Journal of Ethnopharmacology 89, 261–264. https://doi.org/10.1016/j.jep.2003.08.008.CrossRefGoogle Scholar
Isman, MB and Akhtar, Y (2007) Plant natural products as a source for developing environmentally acceptable insecticides. In Ishaaya, I, Nauen, R and Horowitz, AR (eds), Insecticides Design Using Advanced Technologies. Berlin, Heidelberg: Springer, pp. 235–248.CrossRefGoogle Scholar
Isman, MB and Tak, JH (2017) Inhibition of acetylcholinesterase by essential oils and monoterpenoids: a relevant mode of action for insecticidal essential oils? Biopesticides International 13, 71–78.Google Scholar
Jankowska, M, Rogalska, J, Wyszkowska, J and Stankiewicz, M (2018) Molecular targets for components of essential oils in the insect nervous system – a review. Molecules 23, 34. https://doi:10.3390/molecules23010034.CrossRefGoogle Scholar
Jung, HA, Min, B-S, Yokozawa, T, Lee, J-H, Kim, YS and Choi, JS (2009) Anti-Alzheimer and antioxidant activities of Coptidis rhizoma alkaloids. Biological and Pharmaceutical Bulletin 32, 1433–1438.CrossRefGoogle ScholarPubMed
Kim, SI, Roh, JY, Kim, DH, Lee, HS and Ahn, YJ (2003) Insecticidal activities of aromatic plant extracts and essential oils against Sitophilus oryzae and Callosobruchus chinensis. Journal of Stored Products Research 39, 293–303. https://doi.org/10.1016/S0022-474X(02)00017-6.CrossRefGoogle Scholar
Kim, SW, Kang, J and Park, IK (2013) Fumigant toxicity of Apiaceae essential oils and their constituents against Sitophilus oryzae and their acetylcholinesterase inhibitory activity. Journal of Asia-Pacific Entomology 16, 443–447. https://doi.org/10.1016/j.aspen.2013.07.002.CrossRefGoogle Scholar
Klys, M, Malejky, N and Nowak-Chmura, M (2017) The repellent effect of plants and their active substances against the beetle storage pests. Journal of Stored Products Research 74, 66–77. https://doi.org/10.1016/j.jspr.2017.10.006.CrossRefGoogle Scholar
Kordali, S, Yildirim, E, Yazici, G, Emsen, B, Kabaagac, G and Ercisli, S (2012) Fumigant toxicity of essential oils of nine plant species from Asteraceae and Clusiaceae against Sitophilus granarius (L.) (Coleoptera: Curculionidae). Egyptian Journal of Biological Pest Control 22, 11–14.Google Scholar
Kostyukovsky, M, Rafaeli, A, Gileadi, C, Demchenko, N and Shaaya, E (2002) Activation of octopaminergic receptors by essential oil constituents isolate from aromatic plants: possible mode of action against insect pest. Pest Management Science 58, 1101–1106. https://doi.org/10.1002/ps.548.CrossRefGoogle Scholar
Koul, O, Smirle, M and Isman, M (1990) Asarones from Acorus calamus oil: their effect on feeding behavior and dietary utilization in Peridroma saucia. Journal of Chemical Ecology 16, 1911–1920.CrossRefGoogle Scholar
Kumar, P, Mishra, S, Malik, A and Satya, S (2012) Compositional analysis and insecticidal activity of Eucalyptus globulus (family: Myrtaceae) essential oil against housefly (Musca domestica). Acta Tropica 122, 212–218. https://doi.org/10.1016/j.actatropica.2012.01.015.CrossRefGoogle Scholar
Lee, S, Peterson, CJ and Coats, JR (2003) Fumigation toxicity of monoterpenoids to several stored product insects. Journal of Stored Products Research 39, 77–85. https://doi.org/10.1016/S0022-474X(02)00020-6.CrossRefGoogle Scholar
Lee, HR, Kim, GH, Choi, WS and Park, IK (2017) Repellent activity of Apiaceae plant essential oils and their constituents against adult German cockroaches. Journal of Economic Entomology 110, 552–557. https://doi.org/10.1093/jee/tow290.CrossRefGoogle ScholarPubMed
Liu, ZL and Ho, SH (1999) Bioactivity of the essential oil extracted from Evodia rutaecarpa Hook f. et Thomas against the grain storage insects, Sitophilus zeamais Motsch. and Tribolium castaneum (Herbst). Journal of Stored Products Research 35, 317–328. https://doi:10.1016/S0022-474X(99)00015-6.CrossRefGoogle Scholar
Liu, ZL, Chu, SS and Jiang, GH (2011) Insecticidal activity and composition of essential oil of Ostericum sieboldii (Apiaceae) against Sitophilus zeamais and Tribolium castaneum. Records of Natural Products 5, 74–81.Google Scholar
López, MD and Pascual-Villalobos, MJ (2010) Mode of inhibition of acetylcholinesterase by monoterpenoids and implications for pest control. Industrial Crops and Products 31, 284–288. https://doi.org/10.1016/j.indcrop.2009.11.005.CrossRefGoogle Scholar
López, MD, Contreras, J and Pascual-Villalobos, MJ (2010) Selection for tolerance to volatile monoterpenoids in Sitophilus oryzae (L.), Rhyzopertha dominica (F.) and Cryptolestes pusillus (Schoenherr). Journal of Stored Products Research 46, 52–58. https://doi.org/10.1016/j.jspr.2009.09.003.CrossRefGoogle Scholar
López, SB, López, ML, Aragón, LM, Tereschuk, ML, Slanis, AC, Feresin, GE, Zygadlo, JA and Tapia, AA (2011) Composition and anti-insect activity of essential oils from Tagetes l. species (Asteraceae, Helenieae) on Ceratitis capitata Wiedemann and Triatoma infestans Klug. Journal of Agricultural and Food Chemistry 59, 5286–5292. https://doi.org10.1021/jf104966b.CrossRefGoogle ScholarPubMed
Magan, N, Hope, R, Cairns, V and Aldred, D (2003) Postharvest fungal ecology: impact of fungal growth and mycotoxin accumulation in stored grain. European Journal of Plant Pathology 109, 723–730. https://doi.org/10.1023/A:1026082425177.CrossRefGoogle Scholar
Maroufpoor, M, Ebadollahi, A, Vafaee, Y and Badiee, E (2016) Chemical composition and toxicity of the essential oil of Coriandrum sativum L. and Petroselinum crispum L. against three Stored-Product insect pests. Journal of Essential Oil Bearing Plants 19, 1993–2002. https://doi.org/10.1080/0972060X.2016.1256234.CrossRefGoogle Scholar
Massango, HGLL, Faroni, LRA, Haddi, K, Heleno, FF, Jumbo, LOV and Oliveira, EE (2016) Toxicity and metabolic mechanisms underlying the insecticidal activity of parsley essential oil on bean weevil, Callosobruchus macuatus. Journal of Pest Science 90, 723–733. https://doi.org/10.1007/s10340-016-0826-8.CrossRefGoogle Scholar
Ojo, JA and Omoloye, AA (2016) Development and life history of Sitophilus zeamais (Coleoptera: Curculionidae) on cereal crops. Advances in Agriculture 2016, 1–8. https://dx.doi.org/10.1155/2016/7836379.CrossRefGoogle Scholar
Orhan, IE, Senol, FS, Ozturk, N, Celik, SA, Pulur, A and Kan, Y (2013) Phytochemical contents and enzyme inhibitory and antioxidant properties of Anethum graveolens L. (dill) samples cultivated under organic and conventional agricultural conditions. Food and Chemical Toxicology 59, 96–103. https://doi:10.1016/j.fct.2013.05.053.CrossRefGoogle ScholarPubMed
Pavela, R and Vrchotová, N (2013) Insecticidal effect of furanocoumarins from fruits of Angelica archangelica L. against larvae Spodoptera littoralis Boisd. Industrial Crops and Products 43, 33–39. https//doi.org10.1016/j.indcrop.2012.06.044.CrossRefGoogle Scholar
Rattan, RS (2010) Mechanism of action of insecticidal secondary metabolites of plant origin. Crop Protection 29, 913–920. https://doi.org/10.1016/j.cropro.2010.05.008.CrossRefGoogle Scholar
Regnault-Roger, C, Vincent, C and Arnason, JT (2012) Essential oils in insect control: low-risk products in a high-stakes world. Annual Review of Entomology 57, 405–424. https://doi.org/10.1146/annurev-ento-120710-100554.CrossRefGoogle Scholar
Santos, TC, Gomes, TM, Pinto, BAS, Camara, AL and Paes, AMA (2018) Naturally occurring acetylcholinesterase inhibitors and their potential use for Alzheimer's disease therapy. Frontiers in Pharmacology 9, 1192.CrossRefGoogle ScholarPubMed
Scriber, JM and Slansky, F Jr (1981) The nutritional ecology of immature insects. Annual Review of Entomology 26, 183–211. https://doi:10.1146/annurev.en.26.010181.001151.CrossRefGoogle Scholar
Senthil-Nathan, S, Chung, PG and Murugan, K (2005) Effect of biopesticides applied separately or together on nutritional indices of the rice leaf folder Cnaphalocrocis medinalis. Phytoparasitica 33, 187–195. https://doi.org/10.1007/BF03029978.CrossRefGoogle Scholar
Seo, SM, Jung, CS, Kang, J, Lee, HR, Kim, SW, Hyun, J and Park, IK (2015) Larvicidal and acetylcholinesterase inhibitory activity of Apiaceae plant essential oils and their constituents against Aedes albopictus, and formulation development. Journal of Agricultural and Food Chemistry 63, 9977–9986. https://doi:10.1021/acs.jafc.5b03586.CrossRefGoogle ScholarPubMed
Sousa, RMOF, Rosa, JS, Oliveira, L, Cunha, A and Fernandes-Ferreira, M (2013) Activities of Apiaceae essential oils activities against armyworm, Pseudaletia unipuncta (Lepidoptera: Noctuidae). Journal of Agricultural and Food Chemistry 61, 7661–7672. https://doi:10.1021/jf403096d.CrossRefGoogle Scholar
Sousa, RMOF, Rosa, JS, Oliveira, L, Cunha, A and Fernandes-Ferreira, M (2015 a) Activities of Apiaceae essential oils and volatile compounds on hatchability, development, reproduction and nutrition of Pseudaletia unipuncta (Lepidoptera: Noctuidae). Industrial Crops and Products 63, 226–237. https://doi:10.1016/j.indcrop.2014.09.052.CrossRefGoogle Scholar
Sousa, RMOF, Rosa, JS, Silva, CA, Almeida, MTM, Novo, MT, Cunha, AC and Fernandes-Ferreira, M (2015 b) Larvicidal, molluscicidal and nematicidal activities of essential oils and compounds from Foeniculum vulgare. Journal of Pest Science 88, 413–426. htpps://doi:10.1007/s10340-014-0628-9.CrossRefGoogle Scholar
Sousa, RMOF, Rosa, JS, Cunha, AC and Fernandes-Ferreira, M (2017) Molluscicidal activity of four Apiaceae essential oils against the freshwater snail Radix peregra. Journal of Pest Science 90, 971–984. https://doi.org/10.1007/s10340-017-0842-3.CrossRefGoogle Scholar
Stefanazzi, N, Stadler, T and 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, 639–646. https://doi:10.1002/ps.2102.CrossRefGoogle Scholar
Tripathi, AK, Prajapati, V, Aggarwal, KK, Khanuja, SPS and Kumar, S (2000) Repellency and toxicity of oil from Artemisia annua to certain stored-product beetles. Journal of Economic Entomology 93, 43–47. https://doi.org/10.1603/0022-0493-93.1.43.CrossRefGoogle ScholarPubMed
Tripathi, AL, Upadhyay, S, Bhuiyan, M and Bhattacharya, PR (2009) A review on prospects of essential oils as biopesticide in insect-pest management. Journal of Pharmacognosy and Phytotherapy 1, 52–63.Google Scholar
Wang, JL, Li, Y and Lei, CL (2009) Evaluation of monoterpenes for the control of Tribolium castaneum (Herbst) and Sitophilus zeamais Motschulsky. Natural Product Research 23, 1080–1088. https://doi.org/10.1080/14786410802267759.CrossRefGoogle Scholar
Yang, K, Zhou, YX, Wang, CF, Du, SS, Deng, ZW, Liu, QZ and Liu, ZL (2011) Toxicity of Rhododendron anthopogonoides essential oil and its constituent compounds towards Sitophilus zeamais. Molecules 16, 7320–7330. https://doi.org/10.3390/molecules16097320.CrossRefGoogle ScholarPubMed
Yazdani, E, Sendi, JJ, Aliakbar, A and Senthil-Nathan, S (2013) Effect of Lavandula angustifolia essential oil against lesser mulberry pyralid Glyphodes pyloalis Walker (Lep: Pyralidae) and identification of its major derivatives. Pesticide Biochemistry and Physiology 107, 250–257. https://doi.org/10.1016/j.pestbp.2013.08.002.CrossRefGoogle Scholar
Yeom, HJ, Kang, JS, Kim, GH and Park, IK (2012) Insecticidal and acetylcholine esterase inhibition activity of Apiaceae plant essential oils and their constituents against adults of German cockroach (Blattella germanica). Journal of Agricultural and Food Chemistry 60, 7194–7203. https://doi:10.1021/jf302009w.CrossRefGoogle Scholar
Yildirim, E, Emsen, B and Kordali, S (2013) Insecticidal effects of monoterpenes on Sitophilus zeamais Motschulsky (Coleoptera: Curculionidae). Journal of Applied Botany and Food Quality 86, 198–204. https://doi:10.5073/JABFQ.2013.086.027.Google Scholar