Abstract
The aim of this study was to test the effectiveness of essential oils form Piper aduncum, Melaleuca leucadendra and Schinus terebinthifolius and their blends by fumigation and residual contact on Tetranychus urticae and its natural enemy, Neoseiulus californicus. Bioassays were performed in a greenhouse with the best blend of the oils and compared to the individual oils and Vertimec® (positive control). The main constituents identified by GC–MS were dillapiole, (E)-nerolidol and limonene in the oils from P. aduncum (76.5%), M. leucadendra (87.3%) and S. terebinthifolius (unripe/ripe fruits, 42.5/34.1%). The P. aduncum and M. leucadendra oils were the most toxic to the pest. Among the blends, the greatest toxicity to T. urticae occurred by residual contact with the M. leucadendra + S. terebinthifolius ripe fruit blend (50/50). The evaluation of the effects on N. californicus showed the compatibility of the oils and blends with the predator mite for use in the integrated management of T. urticae. β-Caryophyllene was the most toxic, independent of the method used. Based on toxicities of 11 oil constituents, the structure–activity relationship of these compounds is also discussed. This study showed that the acaricidal effect of the Piper, Melaleuca and Schinus oils can easily be increased by the binary combination of these oils. The binary blend between the oils of the Melaleuca leaves and ripe Schinus fruit in the greenhouse was effective at controlling the mite after 72 h, exhibiting the same level of toxicity as that found for the positive control (Vertimec 18 EC).
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Adjalian E, Sessou P, Yehouenou B, Bothon FTD, Noudogbessi JP, Kossou D, Menut C, Sohounhloue D (2015) Anti-oviposition and repellent activity of essential oil from Melaleuca leucadendron leaf acclimated in Bénin against the angoumois grain moth. Int J Biol 4:797–806
Akhtar Y, Isman MB (2013) Plant natural products for pest management: the magic of mixtures. In: Ishaaya I, Palli SR, Horowitz AR (eds) Advanced technologies for managing insect pests. Springer, New York, pp 231–247
Akhtar Y, Pages E, Stevens A, Bradbury R, da Camara CAG, Isman MB (2012) Effect of chemical complexity of essential oils on feeding deterrence in larvae of the cabbage looper. Physiol Entomol 37:81–91. https://doi.org/10.1111/j.1365-3032.2011.00824.x
APRD (2018) Arthropod Pesticide Resistance Database. https://www.pesticideresistance.org/display.php?page=species&arId=536. Accessed 26 Feb 2019.
Araújo MJC, da Camara CAG, Born FS, Moraes MM, Badji CA (2012) Acaricidal activity and repellency of essential oil from Piper aduncum and its components against Tetranychus urticae. Exp Appl Acarol 57:139–155. https://doi.org/10.1007/s10493-012-9545-x
Attia S, Grissa KL, Lognay G, Heuskin S, Mailleux AC, Hance T (2011) Chemical composition and acaricidal properties of Deverra scoparia essential oil (Araliales: Apiaceae) and blends of its major constituents against Tetranychus urticae (Acari: Tetranychidae). J Econ Entomol 104:1220–1228. https://doi.org/10.1603/EC10318
Badawy MEI, El-Arami SAA, Abdelgaleil SAM (2010) Acaricidal and quantitative structure activity relationship of monoterpenes against the two-spotted spider mite, Tetranychus urticae. Exp Appl Acarol 52:261–274. https://doi.org/10.1007/s10493-010-9363-y
Bassolé IHN, Lamien-Meda A, Bayala B, Tirogo S, Franz C, Novak J, Nebié RC, Dicko MH (2010) Composition and antimicrobial activities of Lippia multiflora Moldenke, Mentha × piperita L. and Ocimum basilicum L. essential oils and their major monoterpene alcohols alone and in combination. Molecules 15:7825–7839. https://doi.org/10.3390/molecules15117825
Benelli G, Pavela R, Iannarelli R, Petrelli R, Cappellacci L, Cianfaglione K, Afshar FH, Nicoletti M, Canale A, Maggi F (2017) Synergized mixtures of Apiaceae essential oils and related plant-borne compounds: larvicidal effectiveness on the filariasis vector Culex quinquefasciatus Say. Ind Crop Prod 96:186–195. https://doi.org/10.1016/j.indcrop.2016.11.059
Born FS, da Camara CAG, Melo JPR, Moraes MM (2018) Acaricidal property of the essential oil from Lippia gracilis against Tetranychus urticae and a natural enemy, Neoseiulus californicus, under greenhouse conditions. Exp Appl Acarol 75:491–502. https://doi.org/10.1007/s10493-018-0286-3
Bozhgani NSS, Kheradmand K, Talebi AA (2018) The effects of spirotetramat on the demographic parameters of Neoseiulus californicus (Phytoseiidae). Syst Appl Acarol 23:1952–1964. https://doi.org/10.11158/saa.23.10.7
Cordeiro EMG, Moura ILT, Fadini MAM, Guedes RNC (2013) Beyond selectivity: are behavioral avoidance and hormesis likely causes of pyrethroid-induced outbreaks of the southern red mite Oligonychus ilicis? Chemosphere 93:1111–1116. https://doi.org/10.1016/j.chemosphere.2013.06.030
Da Camara CAG, Akhtar Y, Isman MB, Seffrin RC, Born FS (2015) Repellent activity of essential oils from two species of Citrus against Tetranychus urticae in the laboratory and greenhouse. Crop Prot 74:110–115. https://doi.org/10.1016/j.cropro.2015.04.014
Da Camara CAG, Moraes MM, Melo JPR, Silva MMC (2017) Chemical composition and acaricidal activity of essential oils from Croton rhamnifolioides Pax and Hoffm. in different regions of a caatinga biome in northeastern Brazil. J Essent Oil Bear Plant 20:1434–1449. https://doi.org/10.1080/0972060X.2017.1416677
Dawidar AM, Abdel-Mogib M, El-Naggar ME, Mostafa ME (2009) Chemical constituents and miticidal activity of Ecballium elaterium and Schinus terebinthifolius against Tetranychus urticae Koch. Mans J Chem 36:1–17
De Oliveira ACAX, Ribeiro-Pinto LF, Paumgartten FJR (1997) In vitro inhibition of CYP2B1 monooxygenase by β-myrcene and other monoterpenoid compounds. Toxicol Lett 92:39–46. https://doi.org/10.1016/S0378-4274(97)00034-9
Domingos AC, Melo JWS, Oliveira JEM, Gondim JMGC (2014) Mites on grapevines in northeast Brazil: occurrence, population dynamics and within-plant distribution. Int J Acarol 40:145–151. https://doi.org/10.1080/01647954.2014.891651
Efrom CFS, Redaelli LR, Meirelles RN, Ourique CB (2012) Side-effects of pesticides used in the organic system of production on Apis melífera Linnaeus, 1758. Braz Arch Biol Technol 55:47–53. https://doi.org/10.1590/S1516-89132012000100005
Enan E (2001) Insecticidal activity of essential oils: octopaminergic sites of action. Comp Biochem Physiol C 130:325–337. https://doi.org/10.1016/S1532-0456(01)00255-1
Fadini MAM, Pallini A, Venzon M, Oliveira CM (2009) Uso de ácaros predadores para o controle biológico de ácaros-praga. Informe Agropecuário 30:34–40
Fatemikia S, Abbasipour H, Saeedizadeh A (2017) Phytochemical and acaricidal study of the galbanum, Ferula gumosa Boiss. (Apiaceae) essential oil against Tetranychus urticae Koch (Tetranychidae). J Essent Oil Bear Plant 20:185–195. https://doi.org/10.1080/0972060X.2016.1257957
Han J, Choi BR, Lee SG, Kim SI, Ahn YJ (2010) Toxicity of plant essential oils to acaricide-susceptible and -resistant Tetranychus urticae (Acari: Tetranychidae) and Neoseiulus californicus (Acari: Phytoseiidae). J Econ Entomol 103:1293–1298. https://doi.org/10.1603/EC09222
Harris R (2002) Synergism in the essential oil world. Int J Aromather 12:179–186. https://doi.org/10.1016/S0962-4562(02)00083-8
Hassan SA, Bigler F, Blasisinger P, Bogenschütz H, Brun J, Chiverton P, Dickler E, Easterbrook MA, Edwards PJ, Englert WD, Firth SI, Huang P, Inglesfield C, Klingauf F, Kühner C, Ledieu MS, Naton E, Oomen PA, Overmeer WPJ, Plevoets P, Reboulet JN, Rieckmann W, Samsoe-Petersen L, Shires SW, Stäubli A, Stevenson J, Tuset JJ, Vanwetswinkel G, Van Zon AQ (1985) Standard methods to test the side-effects of pesticides on natural enemies of insects and mites developed by the IOBC/WPRS Working Group ‘Pesticides and Beneficial Organisms’. EPPO Bull 15:214–255. https://doi.org/10.1111/j.1365-2338.1985.tb00224.x
Hussein HS, Salem MZM, Soliman AM (2017) Repellent, attractive, and insecticidal effects of essential oils from Schinus terebinthifolius fruits and Corymbia citriodora leaves on two whitefly species, Bemisia tabaci, and Trialeurodes ricini. Sci Hortic 216:111–119. https://doi.org/10.1016/j.scienta.2017.01.004
Isman MB, Miresmailli S, Machial C (2011) Commercial opportunities for pesticides based on plant essential oils in agriculture, industry and consumer products. Phytochem Rev 10:197–204. https://doi.org/10.1007/s11101-010-9170-4
Jin P, Tian L, Chen L, Hong X (2018) Spider mites of agricultural importance in China, with focus on species composition during the last decade (2008–2017). Syst Appl Acarol 23:2087–2098. https://doi.org/10.11158/saa.23.11.1
Kaufmann D, Dogra AK, Wink M (2011) Myrtenal inhibits acetylcholinesterase, a known Alzheimer target. J Pharm Pharmacol 63:1368–1371. https://doi.org/10.1111/j.2042-7158.2011.01344.x
Kim EH, Kim HK, Ahn YJ (2003) Acaricidal activity of clove bud oil compounds against Dermatophagoides farinae and Dermatophagoides pteronyssinus (Acari: Pyroglyphidae). J Agric Food Chem 51:885–889. https://doi.org/10.1021/jf0208278
Kim SY, Ahn HG, Ha PJ, Lim UT, Lee JH (2018) Toxicities of 26 pesticides against 10 biological control species. J Asia Pac Entomol 21:1–8. https://doi.org/10.1016/j.aspen.2017.10.015
Kumral NA, Çobanoglu S, Yalcin C (2010) Acaricidal, repellent and oviposition deterrent activities of Datura stramonium L. against adult Tetranychus urticae (Koch). J Pest Sci 83:173–180. https://doi.org/10.1007/s10340-009-0284-7
Laborda R, Manzano I, Gamón M, Gavidia I, Pérez-Bermúdez P, Boluda R (2013) Effects of Rosmarinus officinalis and Salvia officinalis essential oils on Tetranychus urticae Koch (Acari: Tetranychidae). Ind Crop Prod 48:106–110. https://doi.org/10.1016/j.indcrop.2013.04.011
Lim EG, Roh HS, Coudron TA, Park CG (2011) Temperature-dependent fumigant activity of essential oils against twospotted spider mite (Acari: Tetranychidae). J Econ Entomol 104:414–419. https://doi.org/10.1603/EC10249
Lucia A, Audino PG, Seccacini E, Licastro S, Zerba E, Masuh H (2007) Larvicidal effect of Eucalyptus grandis essential oil and turpentine and their major components on Aedes aegypti larvae. J Am Mosq Control Assoc 23:299–304. https://doi.org/10.2987/8756-971x(2007)23[299:leoege]2.0.co;2
Lumaret JP, Errouissi F, Floate K, Römbke J, Wardhaugh K (2012) A review on the toxicity and non-target effects of macrocyclic lactones in terrestrial and aquatic environments. Curr Pharm Biotechnol 13:1004–1060. https://doi.org/10.2174/138920112800399257
Mamood SNH, Hidayatulfathi O, Budin SB, Rohi GA, Zulfakar MH (2016) The formulation of the essential oil of Piper aduncum Linnaeus (Piperales: Piperaceae) increases its efficacy as an insect repellent. Bull Entomol Res 107:49–57. https://doi.org/10.1017/S0007485316000614
Mar JM, Silva LS, Azevedo SG, França LP, Goes AFF, Santos AL, Bezerra JA, Nunomura RC, Machado MB, Sanches EA (2018) Lippia origanoides essential oil: an efficient alternative to control Aedes aegypti, Tetranychus urticae and Cerataphis lataniae. Ind Crop Prod 111:292–297. https://doi.org/10.1016/j.indcrop.2017.10.033
Migeon A, Tixier M, Navajas M, Litskas VD, Stavrinides MC (2019) A predator-prey system: Phytoseiulus persimilis (Acari: Phytoseiidae) and Tetranychus urticae (Acari: Tetranychidae): worldwide occurrence datasets. Acarologia 59:301–307. https://doi.org/10.24349/acarologia/20194322
Miresmailli S, Isman MB (2006) Efficacy and persistence of rosemary oil as an acaricide against twospotted spider mite (Acari: Tetranychidae) on greenhouse tomato. J Econ Entomol 99:2015–2023. https://doi.org/10.1093/jee/99.6.2015
Momen FM, Rahman HAA, Sammour EA, Aly SM, Fahim SF (2014) Acaricidal activity of Melissa officinalis oil and its formulation on Tetranychus urticae and the predatory mite Neoseiulus californicus (Acari: Tetranychidae and Phytoseiidae). Acta Phytopathol Entomol Hung 49:95–115. https://doi.org/10.1556/aphyt.49.2014.1.10
Monteiro VB, Gondim JMGC, Oliveira JEM, Siqueira HAA, Sousa JM (2015) Monitoring Tetranychus urticae Koch (Acari: Tetranychidae) resistance to abamectin in vineyards in the Lower Middle São Francisco Valley. Crop Prot 69:90–96. https://doi.org/10.1016/j.cropro.2014.12.012
Moraes MM, da Camara CAG, Santos ML, Fagg CW (2012) Essential oil composition of Eugenia langsdorffii O. Berg.: relationships between some terpenoids and toxicity against Tetranychus urticae. J Braz Chem Soc 23:1647–1656. https://doi.org/10.1590/s0103-50532012005000029
Mozaffari F, Abbasipour H, Garjan AS, Saboori A, Mahmoudvand M (2013) Toxicity and oviposition deterrence and repellency of Mentha pulegium (Lamiaceae) essential oils against Tetranychus urticae Koch (Tetranychidae). J Essent Oil Bear Plant 16:575–581. https://doi.org/10.1080/0972060X.2013.854500
Mwaiko GL (1992) Citrus peel oil extracts as mosquito larvae insecticide. East Afr Med J 69:223–226
Nascimento AF, da Camara CAG, Moraes MM, Ramos CS (2012) Essential oil composition and acaricidal activity of Schinus terebinthifolius from Atlantic Forest of Pernambuco, Brazil against Tetranychus urticae. Nat Prod Commun 7:129–132
Nascimento AF, da Camara CAG, Moraes MM (2018) Fumigant activity of Schinus terebinthifolius essential oil and its selected constituents against Rhyzopertha dominica. Rev Fac Nac Agron Medellín 71:8359–8366. https://doi.org/10.15446/rfna.v71n1.62743.
Oliveira JCS, Dias IJM, da Camara CAG, Schwartz MOE (2006) Volatile constituents of the leaf oils of Piper aduncum L. from different regions of Pernambuco (Northeast of Brazil). J Essent Oil Res 18:557–559. https://doi.org/10.1080/10412905.2006.9699166
Padalia RC, Verma RS, Chauhan A, Chanotiya CS (2015) The essential oil composition of Melaleuca leucadendra L. grown in India: a novel source of (E)-nerolidol. Ind Crop Prod 69:224–227. https://doi.org/10.1016/j.indcrop.2015.02.019
Pavela R (2015) Acute toxicity and synergistic and antagonistic effects of the aromatic compounds of some essential oils against Culex quinquefasciatus Say larvae. Parasitol Res 114:3835–3853. https://doi.org/10.1007/s00436-015-4614-9
Pereira ACRL, Oliveira JV, Gondim JMGC, da Câmara CAG (2009) Influence of the storage period of cowpea [Vigna unguiculata (L.) Walp.] treated with essential and fixed oils, for the control of Callosobruchus maculatus (Fabricius, 1775) (Coleoptera, Chrysomelidae, Bruchinae). Ciência e Agrotecnologia 33:319–325. https://doi.org/10.1590/S1413-70542009000100044
Perumalsamy H, Kim NJ, Ahn AJ (2009) Larvicidal activity of compounds isolated from Asarum heterotropoides against Culex pipiens pallens, Aedes aegypti, and Ochlerotatus togoi (Diptera: Culicidae). J Med Entomol 46:1420–1423. https://doi.org/10.1603/033.046.0624
Potzernheim MCL, Bizzo HR, Silva JP, Vieira RF (2012) Chemical characterization of essential oil constituents of four populations of Piper aduncum L. from Distrito Federal, Brazil. Biochem Syst Ecol 42:25–31. https://doi.org/10.1016/j.bse.2011.12.025
Ribeiro N, da Camara CAG, Ramos C (2016) Toxicity of essential oils of Piper marginatum Jacq. against Tetranychus urticae Koch and Neoseiulus californicus (McGregor). Chilean J Agric Res 76:71–76. https://doi.org/10.4067/s0718-58392016000100010
Sánchez-Ramos I, Castañera P (2001) Acaricidal activity of natural monoterpenes on Tyrophagus putrescentiae (Schrank), a mite of stored food. J Stored Prod Res 37:93–101. https://doi.org/10.1016/s0022-474x(00)00012-6
Sanini C, Massarolli A, Krinski D, Butnariu AR (2017) Essential oil of spiked pepper, Piper aduncum L. (Piperaceae), for the control of caterpillar soybean looper, Chrysodeixis includens Walker (Lepidoptera: Noctuidae). Braz J Bot 40:399–404. https://doi.org/10.1007/s40415-017-0363-6
Santos SRL, Silva VB, Melo MA, Barbosa JDF, Santos RLC, Souza DP, Cavalcanti SCH (2010) Toxic effects on and structure-toxicity relationships of phenylpropanoids, terpenes, and related compounds in Aedes aegypti larvae. Vector Borne Zoonotic Dis 10:1049–1054. https://doi.org/10.1089/vbz.2009.0158
SAS Institute (2002) SAS User’s guide: Statistics, Version 9.0, 7th edn. SAS Institute Inc, Cary, North Carolina.
Sato ME, Silva MZ, Filho MFS, Matioli AL, Raga A (2007) Management of Tetranychus urticae (Acari: Tetranychidae) in strawberry fields with Neoseiulus californicus (Acari: Phytoseiidae) and acaricides. Exp Appl Acarol 42:107–120. https://doi.org/10.1007/s10493-007-9081-2
Schimitberger VMB, Pratti DLA, Cavalcantia LC, RamalhoVF CAPF, Scherer R, Kuster RM, Ramos AC, Silva AG (2018) Volatile compounds profile changes from unripe to ripe fruits of Brazilian pepper (Schinus terebinthifolia Raddi). Ind Crop Prod 119:125–131. https://doi.org/10.1016/j.indcrop.2018.04.011
Shaalan EA, Canyon DV, Younes MW, Abdel-Wahab H, Mansour AH (2005) Effects of sub-lethal concentrations of synthetic insecticides and Callitris glaucophylla extracts on the development of Aedes aegypti. J Vector Ecol 30:295–298
Silva AG, Almeida DL, Ronchi SN, Bento AC, Scherer R, Ramos AC, Cruz ZMA (2010) The essential oil of Brazilian pepper, Schinus terebinthifolia Raddi in larval control of Stegomyia aegypti (Linnaeus, 1762). Parasit Vector 3:1–7. https://doi.org/10.1186/1756-3305-3-79
Song JE, Kim JM, Lee NH, Yang JY, Lee HS (2016) Acaricidal and insecticidal activities of essential oils against a stored-food mite and stored-grain insects. J Food Prot 79:174–178. https://doi.org/10.4315/0362-028X.JFP-15-109
Tak JH, Jovel E, Isman MB (2016) Contact, fumigant, and cytotoxic activities of thyme and lemongrass essential oils against larvae and an ovarian cell line of the cabbage looper, Trichoplusia ni. J Pest Sci 89:183–193. https://doi.org/10.1007/s10340-015-0655-1
Vassiliou VA, Kitsis P (2013) Acaricide resistance in Tetranychus urticae (Acari: Tetranychidae) populations from Cyprus. J Econ Entomol 106:1848–1854. https://doi.org/10.1603/ec12369
Yoon J, Tak JH (2018) Toxicity and repellent activity of plant essential oils and their blending effects against two spotted spider mites, Tetranychus urticae Koch. Korean J Appl Entomol 57:199–207
Acknowledgements
The authors are grateful to Dr. Angela Maria de Miranda Freitas and Dr. Maria Rita Cabral Sales de Melo of the Rural Federal University of Pernambuco for the identification of the plant species used in the study. This work was supported by the FACEPE [APQ-1008-1.06/15; APQ-0476-1.06/14; APQ-08601.06/16; IBPG-0984-5.01/10] and CNPq [PQ-302860/2016-9] for awarding a grant.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
de Araújo, M.J.C., da Câmara, C.A.G., Born, F.S. et al. Acaricidal activity of binary blends of essential oils and selected constituents against Tetranychus urticae in laboratory/greenhouse experiments and the impact on Neoseiulus californicus. Exp Appl Acarol 80, 423–444 (2020). https://doi.org/10.1007/s10493-020-00464-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10493-020-00464-8