Lethal Toxicity of Thymus capitatus Essential Oil Against Planococcus citri (Hemiptera: Pseudococcidae) and its Coccinellid Predator Cryptolaemus montrouzieri (Coleoptera: Coccinellidae)
biocontrol agent; citrus mealybug; fumigant toxicity; natural extracts; Ecology, Evolution, Behavior and Systematics; Agronomy and Crop Science; Insect Science
Abstract :
[en] Botanical extracts, including essential oils, are promising alternatives to synthetic insecticides for pest control. In this study, we evaluated the fumigant toxicity of an essential oil extracted from Thymus capitatus (L.) Hoffmanns. & Link against the citrus mealybug, Planococcus citri Risso (Hemiptera: Pseudococcidae), and its coccinellid predator Cryptolaemus montrouzieri Mulsant (Coleoptera: Coccinellidae) under laboratory conditions. Gas chromatography-mass spectrometry analysis indicated that the major chemical compounds identified from T. capitatus were carvacrol (65.15%), followed by p-cymene (11.79%) and γterpinene (7.48%). High mortality levels were registered for P. citri larvae (up to 100%) and adults (up to 96%) when exposed to the tested essential oil. The median lethal concentration values calculated for P. citri adults were higher than for larvae. Thymus capitatus essential oil applied at 10 and 20 μL/Lair showed high toxicity towards C. montrouzieri adults. These results highlighted the efficacy of T. capitatus essential oil as a promising tool to control P. citri in Tunisia. However, the adverse effects of this oil towards C. montrouzieri should be taken into consideration to enhance its practical implication in integrated pest management.
Disciplines :
Entomology & pest control
Author, co-author :
Alloui-Griza, Rafika; Department of Plant Health and Environment, Laboratory of Bioaggressors and Integrated Pest Management in Agriculture, University of Carthage, National Agronomic Institute of Tunisia, Tunis, Tunisia
Cherif, Asma ; Université de Liège - ULiège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Gestion durable des bio-agresseurs ; Department of Plant Health and Environment, Laboratory of Bioaggressors and Integrated Pest Management in Agriculture, University of Carthage, National Agronomic Institute of Tunisia, Tunis, Tunisia
Attia, Sabrine; Department of Plant Health and Environment, Laboratory of Bioaggressors and Integrated Pest Management in Agriculture, University of Carthage, National Agronomic Institute of Tunisia, Tunis, Tunisia
Francis, Frédéric ; Université de Liège - ULiège > TERRA Research Centre > Gestion durable des bio-agresseurs ; Department of Plant Health and Environment, Laboratory of Bioaggressors and Integrated Pest Management in Agriculture, University of Carthage, National Agronomic Institute of Tunisia, Tunis, Tunisia
Lognay, Georges ; Université de Liège - ULiège > Département des sciences et gestion de l'environnement (Arlon Campus Environnement) > Surveillance de l'environnement ; Department of Plant Health and Environment, Laboratory of Bioaggressors and Integrated Pest Management in Agriculture, University of Carthage, National Agronomic Institute of Tunisia, Tunis, Tunisia
Grissa-Lebdi, Kaouthar; Department of Plant Health and Environment, Laboratory of Bioaggressors and Integrated Pest Management in Agriculture, University of Carthage, National Agronomic Institute of Tunisia, Tunis, Tunisia
Language :
English
Title :
Lethal Toxicity of Thymus capitatus Essential Oil Against Planococcus citri (Hemiptera: Pseudococcidae) and its Coccinellid Predator Cryptolaemus montrouzieri (Coleoptera: Coccinellidae)
This work was supported by the National Agronomic Institute of Tunisia. Rafika Alloui-Griza benefited from a doctoral fellowship as a part of Algerian–Tunisian cooperation from the Ministry of Higher Education and Scientific Research, Algeria.
Adams, R.P. 2001. Identification of essential oils components by gas chromatography mass spectrometry. Allured Publishing Corp. Carol Stream, IL.
Afifi, A.I., S.A. El Arnaouty, A.R. Attia and A.-M. Abd Alla. 2010. Biological control of citrus mealybug, Planococcus citri (Risso) using coccinellid predator, Cryptolaemus montrouzieri Muls. Pak. J. Biol. Sci. 13: 216-222. doi: 10.3923/pjbs.2010.216.222.
Aissaoui, A.B., A. El Amrani, S. Zantar and L. Toukour. 2018. Activite acaricide des huiles essentielles du mentha pulegium, origanum compactum et thymus capitatus sur L'acarien phytophage tetranychus urticae koch (Acari: tetranychidae). Eur. Sci. J. 14: 118. doi: 10. 19044/esj.2018.v14n3p118.
Akrout, A., H. El Jani, S. Amouri and M. Neffati. 2010. Screening of antiradical and antibacterial activities of essential oils of Artemisia campestris L., Artemisia helba Alba Asso, and Thumus capitatus Hoff. et Link. growing wild in the southern of Tunisia. Recent Res. Sci. Technol. 2: 29-39.
Al-Mazra'awi, M. and M.A. Ateyyat. 2009. Insecticidal and repellent activities of medicinal plant extracts against the sweet potato whitefly, Bemisia tabaci (Hom.: Aleyrodidae) and its parasitoid Eretmocerus mundus (Hym.: Aphelinidae). J. Pest. Sci. 82: 149-154.
Attia, S., K.L. Grissa, Z.G. Ghrabi, A.C. Mailleux, G. Lognay and T. Hance. 2012. Acaricidal activity of 31 essential oils extracted from plants collected in Tunisia. J. Essent. Oil Res. 24: 279-288. doi: 10.1080/10412905.2012.676777.
Bakkali-Aissaoui, A. and A. Elamrani. 2020. Toxicity testing of some essential oils on Tetranychus urticae Koch (Acari: Tetranychidae) and predator spider Phytoseiulus persimilis Athias-Henroit (Acari: Phytoseiidae). J. Agric. Environ. Vet. Sci. 4(3): 1-14.
Ben Ghnaya-Chakroun, A., Y. Mastouri, A. Rezgui, J. Vallance, A. Yacoub, P. Rey, N. Sadfi-Zouaoui and L. Hamrouni. 2015. Chemical composition and antifungal activity of Thymus capitatus L. essential oil against the grapevine wood diseases (GTDs Esca and BDA). 5th Conf. Intern. Methodes Alternatives de Protection des Plantes, 11-13 March 2015, Nouceau sie le, Lille, France. pp. 177-185.
Bibi, R., M. Ahmad, A. Gulzar and M. Tariq. 2021. Effect of profenofos and citrus oil on Cryptolaemus montrouzieri Mulsant and Chrysoperla carnea Stephens, key predators of citrus mealybug, Planococcus citri (Risso), under laboratory conditions. Int. J. Trop. Insect. Sci. doi: 10.1007/s42690-021-00555-y.
Blaisdell, G.K., S. Zhang, A. Rowhani, V. Klaassen, M.L. Cooper, K.M. Daane and R.P.P. Almeida. 2020. Trends in vector-borne transmission efficiency from coinfected hosts: grapevine leafroll-associated virus-3 and grapevine virus A. Eur. J. Plant Pathol. 156: 1163-1167. doi: 10.1007/s10658-019-01916-7.
Bodenheimer, F.S. 1951. Citrus Entomology in the Middle East (The Honeydew Moth, Cryptoblabes gnidiella Mill.) with Special References to Egypt, Iran, Iraq, Palestine, Syria and Turkey. Dr. W. Junk Publishers, The Hague, Netherlands.
Bounatirou, S., S. Smiti, M.G. Miguel, L. Faleiro, M.N. Rejeb, M. Neffati, M.M. Costa, A. Figueiredo, J.G. Barroso and L.G. Pedro. 2007. Chemical composition, antioxidant and antibacterial activities of the essential oils isolated from Tunisian Thymus capitatus Hoff. et Link. Food Chem. 105: 146-155.
Bru ck, E., A. Elbert, R. Fischer, S. Krueger, J. Ku hnhold, A.M. Klueken, R. Nauen, J.F. Niebes, U. Reckmann, H.S. Schnorbach, R. Steffens and X. Van Waetermeulen. 2009. MoventoT, an innovative ambimobile insecticide for sucking insect pest control in agriculture: Biological profile and field performance. Crop Prot. 28: 838-844. doi: 10.1016/ j.cropro.2009.06.015.
El-Jalel, L.F.A., W.M. Elkady, M.H. Gonaid and K.A. El-Gareeb. 2018. Difference in chemical composition and antimicrobial activity of Thymus capitatus L. essential oil at different altitudes. Future J. Pharm. Sci. 4: 156-160. doi: 10.1016/j.fjps.2017.12.004.
Erdemir, T. and F. Erler. 2017. Repellent, oviposition-deterrent and egg-hatching inhibitory effects of some plant essential oils against citrus mealybug, Planococcus citri Risso (Hemiptera: Pseudococcidae). J. Plant Dis. Prot. 124: 473-479. doi: 10.1007/s41348-017- 0112-x.
Fand, B.B., R.D. Gautam, A. Kamra, S.S. Suroshe and S. Mohan. 2012. Bioefficacy of aqueous garlic extract and a symbiotic bacterium, Photorhabdus luminescens against Phenacoccus solenopsis Tinsley (Homoptera: Pseudococcidae). Biopestic. Int. 8(1): 38- 48.
Fidan, H., G. Stefanova, I. Kostova, S. Stankov, S. Damyanova, A. Stoyanova and V.D. Zheljazkov. 2019. Chemical composition and antimicrobial activity of Laurus nobilis L. essential oils from Bulgaria. Molecules 24: 804. doi: 10.3390/molecules24040804.
Franco, J.C., A. Zada and Z. Mendel. 2009. Novel approaches for the management of mealybug pests, Pp. 233-278. In Ishaaya, I. and A.R. Horowitz (eds.), Biorational Control of Arthropod Pests. Application and Resistance Management. Springer, Dordrecht, Netherlands. doi: 10.1007/978-90-481-2316-210.
Giweli, A., A. Said, T. Aoun and N. Elhaji. 2016. Allelopathic effects on seeds germination of Lactuca sativa L. seeds and antibacterial activity of Thymus capitatus essential oil from zintan-libiya flora. Am. Sci. Res. J. Eng, Technol. Sci. (ASRJETS) 17(1): 121-131.
Goldasteh, S., A.A Talebi, Y. Fathipour, H. Ostovan, A. Zamani and R.V. Ei Shoushtari. 2009. Effect of temperature on life history and population growth parameters of Planococcus citri (Homoptera, Pseudococcidae) on coleus [Solenostemon scutellarioides (L.) Codd.]. Arch. Biol. Sci. 61: 329-336. doi: 10.2298/ABS0902329G.
Goudjil, M.B., S. Zighmi, D. Hamada, Z. Mahcene, S.E. Bencheikh and S. Ladjel. 2020. Biological activities of essential oils extracted from Thymus capitatus (Lamiaceae). S. Afr. J. Bot. 128: 274-282. doi: 10.1016/j.sajb.2019.11.020.
Hosni, K., I. Hassen, H. Chaabane, M. Jemli, S. Dallali, H. Sebei and H. Casabianca. 2013. Enzyme-assisted extraction of essential oils from thyme (Thymus capitatus L.) and rosemary (Rosmarinus officinalis L.): Impact on yield, chemical composition and antimicrobial activity. Ind. Crops Prod. 47: 291-299. doi: 10.1016/j.indcrop.2013.03.023.
Isman, M.B., J.A.Wilson and R. Bradbury. 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(1-2): 82-87. doi: 10.1080/13880200701734661.
Jacas, J.A., F. Karamaouna, R. Vercher and L. Zappala . 2010. Citrus pest management in the Northern Mediterranean Basin (Spain, Italy and Greece), Pp. 3-27. In Ciancio A. amd K. Mukerji (eds.), Integrated Management of Arthropod Pests and Insect Borne Diseases. Integrated Management of Plant Pests and Diseases. Springer, Dordrecht, Netherlands. doi: 10.1007/978-90-481-8606-81.
Jaouad, M., A. Moinina, S. Ezrar and R. Lahlali. 2020. Key pests and diseases of citrus trees with emphasis on root rot diseases: An overview. Moroccan J. Agric. Sci. 1: 149- 160.
Kairo, M.T.K., O. Paraiso, R.M. Gautam and D.D. Peterkin. 2013. Cryptolaemus montrouzieri (Mulsant) (Coccinellidae: Scymninae): A review of biology, ecology, and use in biological control with particular reference to potential impact on non-target organisms. CAB. Rev. 8(5): 1-20. doi: 10.1079/PAVSNNR20138005.
Kerns, D., G. Wright and J. Loghry. 2001. Citrus mealybug (Planococcus citri ). Citrus arthropod pest management in Arizona, Tucson (85721). 24 December 2021. (https:// cals.arizona.edu/crop/citrus/insects/citrusmealy.pdf ).
Khaled, W., I. Ben Fekih, I. Chaieb, R. Souissi, I. Harbaoui, and S. Boukhris-Bouhachem. 2017. Insecticidal activity assessment of Thymus capitatus essential oils in combination with natural abrasives against Myzus persicae. Tunis. J. Plant Prot. 12: 49-59.
Mansour, R., F.E. Youssfi, K.G. Labdi and S. Rezgui. 2010. Imidacloprid applied through drip irrigation as a new promising alternative to control mealybugs in Tunisian vineyards. J. Plant Prot. Res. 50:314-319. doi: 10.2478/v10045-010-0054-9.
Mishra, M.K., R. Pandey and A.K. Panday. 2021. Promising biological control systems against insect-pests of horticultural crops in India, Pp. 1-203. In Y.K. Mishra, A.K. Panday and A.K. Sharma (eds.), Insect Pest Management Concept and Approaches. AkiNik Publications, New Delhi, India. doi: 10.22271/ed.book.1199.
Mkaddem, M.G., M. Romdhane, H. Ibrahim, M. Ennajar, A. Lebrihi, F. Mathieu and J. Bouajila. 2010. Essential oil of Thymus capitatus Hoff. et Link. from Matmata, Tunisia: Gas chromatography-mass spectrometry analysis and antimicrobial and antioxidant activities. J. Med. Food 13: 1500-1504. doi: 10.1089/jmf.2009.0117.
Morandi Filho, W.J., V.C. Pacheco-Da-Silva, M.C. Granara De Willink, E. Prado and M. Botton. 2015. A survey of mealybugs infesting South-Brazilian wine vineyards. Rev. Bras. Entomol. 59(1): 251-254. doi: 10.1016/j.rbe.2015.05.002.
Moujahed, N., Y. Bouaziz, A.B. Jannet and Z. Ghrabi. 2011. Nutritive value and essential oils characterization of Rosmarinus officinalis and Thymus capitatus from the central region of Tunisia, Pp. 245-249. In Ranilla, M.J., B. CarroMdSalem and P. Morand-Fehr (eds.), Challenging Strategies to Promote the Sheep and Goat Sector in the Current Global Context Options Mediterraneennes. Ciheam-Iamz/Csic/Universidad De Leon/Fao, Zaragoza, Spain.
Msaada, K., M. Ben Taa rit, K. Hosni, N. Salem, S. Tammar, I. Bettaieb, M. Hammami, F. Limam and B. Marzouk. 2012. Comparison of different extraction methods for the determination of essential oils and related compounds from coriander (Coriandrum sativum L.). Acta Chim. Slov. 59: 803-813.
Perez-Rodriguez, J., J.R. Miksanek, J. Selfa, V. Martinez-Blay, A. Soto, A. Urbaneja and A. Tena. 2019. Field evaluation of Cryptolaemus montrouzieri (Mulsant) (Coleoptera: Coccinellidae) as biological control agent of the mealybug Delottococcus aberiae De Lotto (Hemiptera: Pseudococcidae). Biol. Control 138: 1-7 doi: 10.1016/j.biocontrol.2019. 104027.
Rao, C.N., V.J. Shivankar and S. Singh. 2006. Citrus mealy bug (Planococcus citri Risso) management-A review. Agric. Rev. 27: 142-146.
Raveau, R., J. Fontaine and A. Lounes-Hadj Sahraoui. 2020. Essential oils as potential alternative biocontrol products against plant pathogens and weeds. Rev. Food 9: 365. doi: 10.3390/foods9030365.
Regnault-Roger, C., C. Vincent and J.T. Arnason. 2012. Essential oils in insect control: Low-risk products in a high-stakes world. Annu. Rev. Entomol. 57: 405-424.
Rung, A., D.R. Miller and S.J. Scheffer. 2009. Polymerase chain reaction restriction fragment length polymorphism method to distinguish three mealybug groups within the Planococcus citri-P. minor species complex (Hemiptera: Coccoidea: Pseudococcidae). J. Econ. Entomol. 102: 8-12. doi: 10.1603/029.102.0102.
Salama, M.M., E.E. Taher and M.M. El-Bahy. 2012. Molluscicidal and mosquitocidal activities of the essential oils of Thymus capitatus Hoff. et Link. and Marrubium vulgare L. Rev. Inst. Med. Trop. Sao Paulo. 54: 281-286. doi: 10.1590/s0036-46652012000500008.
Saljoqi, A., M. Nasir, J. Khan, E. Ul-Haq, M. Salim, M. Nadeem, Z. Huma, H.G. Saeed, B. Ahmad, H. Zada and S. Rehman. 2015. Functional response study of Cryptolaemus Montrouzieri Mulsant (Coleoptera: Coccinellidae) fed on cotton mealy bug, Phenacoccus Solenopsis Tinsley under laboratory conditions. J. Entomol. Zool. Stud. 3: 411-415.
Santiago, V., E. Bonifaz, A. Alegre and J. Iannacone. 2014. Toxicitede Chenopodium ambrosioides (Amaranthaceae) et Imidaclopride sur Cryptolaemus montrouzieri (Coleoptera : Coccinellidae). Chaise Villarreal 2 (1). doi: 10.24039/cv20142124.
Satar, G., H.F. Atesx and S. Satar. 2013. Effects of different insecticides on life stages of Planococcus citri Risso (Hemiptera: Pseudococcidae). IOBC/WPRS Bull. 95:183-190.
Tammar, S., N. Salem, I. Bettaieb Rebey, J. Sriti, M. Hammami, S. Khammassi, B. Marzouk , R. Ksouri and K. Msaada. 2018. Regional effect on essential oil composition and antimicrobial activity of Thymus capitatus L. J. Essent. Oil Res. 31: 129-137. doi: 10. 1080/10412905.2018.1539415.
Uygun, N. and S. Satar. 2008. The current situation of citrus pests and their control methods in Turkey. IOBC-WPRS. Bull. 38: 2-9.
Venkatesan, T., S.K. Jalali, S.L. Ramya and M. Prathibha. 2016. Insecticide resistance and its management in mealybugs, Pp. 223-229. In Mani, M. and C. Shivaraju (eds.), Mealybugs and Their Management in Agricultural and Horticultural Crops. Springer, New Delhi, India. doi: 10.1007/978-81-322-2677-217.
Wang, J., F. Zhu, X.M. Zhou, C.Y. Niu and C.L. Lei. 2006. Repellent and fumigant activity of essential oil from Artemisia vulgaris to Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae). J. Stored Prod. Res. 42: 339-347. doi: 10.1016/j.jspr.2005.06.001.
Yayla, M., A. Tusun and S. Satar. 2020. The potential of Sympherobius pygmaeus as a biological agent against Planococcus citri in citrus orchards. J. Entomol. Res. Soc. 22: 1- 12.
Zairi, A., S. Nouir, A. Zarrouk, H. Haddad, A. Khelifa, L. Achour, F. Tangy, M. Chaouachi and M. Trabelsi. 2019. Chemical composition, fatty acids profile and biological properties of Thymus capitatus (L.) Hoffmanns, essential oil. Sci. Rep. 9. doi: 10.1038/s41598-019- 56580-y.
Zappala , L. 2010. Citrus integrated pest management in Italy, Pp. 73-100. In Ciancio, A. and K. Mukerji (eds.), Integrated Management of Arthropod Pests And Insect Borne Diseases. Integrated Management of Plant Pests and Diseases. Springer, Dordrecht, Netherlands. doi: 10.1007/978-90-481-8606-84.
