Biochemical mechanisms of acaricidal activity of 2,4-di-tert-butylphenol and ethyl oleate against the carmine spider mite Tetranychus cinnabarinus

  • Yijuan Chen
  • Cédric Bertrand
  • Guanghui Dai
  • Jiaojian Yuan
Original Paper


Tetranychus cinnabarinus (Boisduval) is one of the most economically important and highly polyphagous herbivorous pests in fields and greenhouses worldwide. We previously reported that 2,4-di-tert-butylphenol (DTBP) and ethyl oleate (EO) showed significantly acaricidal, repellent and oviposition deterrent properties against T. cinnabarinus via an unknown mechanism. In this study, the acaricidal activities of DTBP and EO and their biochemical mechanisms in controlling T. cinnabarinus were investigated at different time points by assessing the associated changes in toxic symptoms, potential target-related enzyme activities and seven neurotransmitters belonging to the biogenic amines (BAs). The results showed that the median lethal times (LT50) for DTBP and EO were 8 and 15 h after treatment, respectively. Using dynamic symptomatology observations, typical neurotoxic symptoms including excitation, convulsion and paralysis were observed in the mites treated with DTBP and EO. Furthermore, the two compounds exerted significant inhibitory activity on monoamine oxidase (MAO) in adult T. cinnabarinus females in vitro and in vivo and had little effect on acetylcholinesterase (AChE) activity. The content levels of the seven BAs analyzed by UPLC-3QMS were higher in the mites treated with DTBP and EO than in the controls, except for phenethylamine (PEA) (for DTBP and EO) and octopamine (OA) (for EO). These results demonstrate that both DTBP and EO exert effects on T. cinnabarinus that are possibly consequences of their preventive effects on the deamination of BAs in the nervous system, most likely through inhibitory effects on MAO or MAO-like enzymes and/or interactions with certain special biogenic amine G protein-coupled receptors.


Tetranychus cinnabarinus 2,4-Di-tert-butylphenol Ethyl oleate Biogenic amines Monoamine oxidase 

Supplementary material

10340_2017_847_MOESM1_ESM.doc (64 kb)
Supplementary material 1 (DOC 64 kb)


  1. Adamo SA, Linn CE, Hoy RR (1995) The role of neurohormonal octopamine during “fight or flight” behavior in the field cricket Gryllus bimaculatus. J Exp Biol 198:1691–1700PubMedGoogle Scholar
  2. Aker WG, Hu X, Wang P, Hwang HM (2008) Comparing the relative toxicity of malathion and malaoxon in blue catfish Ictalurus furcatus. Environ Toxicol 23:548–554CrossRefPubMedGoogle Scholar
  3. Anderson JA, Coats JR (2012) Acetylcholinesterase inhibition by nootkatone and carvacrol in arthropods. Pestic Biochem Physiol 102:124–128CrossRefGoogle Scholar
  4. Attia S, Grissa KL, Lognay G, Bitume E, Hance T, Mailleux AC (2013) A review of the major biological approaches to control the worldwide pest Tetranychus urticae (Acari: Tetranychidae) with special reference to natural pesticides. J Pest Sci 86:361–386CrossRefGoogle Scholar
  5. Auger P, Migeon A, Ueckermann EA, Tiedt L, Navajas M (2013) Evidence for synonymy between Tetranychus urticae and Tetranychus cinnabarinus (Acari, prostigmata, tetranychidae): review and new data. Acarologia 53:383–415CrossRefGoogle Scholar
  6. Ay R, Yorulmaz S (2010) Inheritance and detoxification enzyme levels in Tetranychus urticae Koch (Acari: Tetranychidae) strain selected with chlorpyrifos. J Pest Sci 83:85–93CrossRefGoogle Scholar
  7. Aziz SA, Knowles CO (1973) Inhibition of monoamine oxidase by the pesticide chlordimeform and related compounds. Nature 242:417–418CrossRefPubMedGoogle Scholar
  8. Beeman RW, Matsumura F (1973) Chlordimeform: a pesticide acting upon amine regulatory mechanisms. Nature 242:273–274CrossRefPubMedGoogle Scholar
  9. Blenau W, Baumann A (2001) Molecular and pharmacological properties of insect biogenic amine receptors: lessons from Drosophila melanogaster and Apis mellifera. Arch Insect Biochem Physiol 48:13–38CrossRefPubMedGoogle Scholar
  10. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefPubMedGoogle Scholar
  11. Bu CY, Peng B, Cao Y, Wang XQ, Chen Q, Li JL, Shi GL (2015) Novel and selective acetylcholinesterase inhibitors for Tetranychus cinnabarinus (Acari: Tetranychidae). Insect Biochem Mol Biol 66:129–135CrossRefPubMedGoogle Scholar
  12. Casida JE, Durkin KA (2013) Neuroactive insecticides: targets, selectivity, resistance, and secondary effects. Annu Rev Entomol 58:99–117CrossRefPubMedGoogle Scholar
  13. Chen YJ, Dai GH (2015a) Acaricidal activity of compounds from Cinnamomum camphora (L.) Presl against the carmine spider mite, Tetranychus cinnabarinus. Pest Manag Sci 71:1561–1571CrossRefPubMedGoogle Scholar
  14. Chen YJ, Dai GH (2015b) Acaricidal, repellent, and oviposition-deterrent activities of 2,4-di-tert- butylphenol and ethyl oleate against the carmine spider mite Tetranychus cinnabarinus. J Pest Sci 88:645–655CrossRefGoogle Scholar
  15. Chuah TS, Norhafizah MZ, Ismail S (2014) Phytotoxic effects of the extracts and compounds isolated from napiergrass (Pennisetum purpureum) on chinese sprangletop (Leptochloa chinensis) germination and seedling growth in aerobic rice systems. Weed Sci 62:457–467CrossRefGoogle Scholar
  16. Copping LG, Duke SO (2007) Natural products that have been used commercially as crop protection agents. Pest Manag Sci 63:524–554CrossRefPubMedGoogle Scholar
  17. Dekeyser MA (2005) Acaricide mode of action. Pest Manag Sci 61:103–110CrossRefPubMedGoogle Scholar
  18. Del Pino J, Martínez MA, Castellano V, Ramos E, Martínez-Larrañaga MR, Anadón A (2013) Effects of exposure to amitraz on noradrenaline, serotonin and dopamine levels in brain regions of 30 and 60 days old male rats. Toxicology 308:88–95CrossRefPubMedGoogle Scholar
  19. Dharni S, Sanchita, Maurya A, Samad A, Srivastava SK, Sharma A, Patra DD (2014) Purification, characterization, and in vitro activity of 2,4-di-tert-butylphenol from Pseudomonas monteilii PsF84: conformational and molecular docking studies. J Agric Food Chem 62:6138–6146CrossRefPubMedGoogle Scholar
  20. Edwards DH, Kravitz EA (1997) Serotonin, social status and aggression. Curr Opin Neurobiol 7:812–819CrossRefPubMedGoogle Scholar
  21. El-Kholy S, Stephano F, Li Y, Bhandari A, Fink C, Roeder T (2015) Expression analysis of octopamine and tyramine receptors in Drosophila. Cell Tissue Res 361:669–684CrossRefPubMedGoogle Scholar
  22. Ellman GL, Coutny KD, Andres U, Featherstone KM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95CrossRefPubMedGoogle Scholar
  23. Erber J, Kloppenburg P (1995) The modulatory effects of serotonin and octopamine in the visual system of the honey bee (Apis mellifera L.). I. Behavioral analysis of the motion-sensitive antennal reflex. J Comp Physiol 176:111–118CrossRefGoogle Scholar
  24. Flório JC, Sakate M, Palemo-Neto J (1993) Effects of amitraz on motor function. Pharmacol Toxicol 73:109–114CrossRefPubMedGoogle Scholar
  25. Grbić M, Van Leeuwen T, Clark RM, Rombauts S, Rouzé P, Grbić V, Osborne EJ et al (2011) The genome of Tetranychus urticae reveals herbivorous pest adaptations. Nature 479:487–492CrossRefPubMedPubMedCentralGoogle Scholar
  26. Gruntenko NE, Chentsova NA, Bogomolova EV, Karpova EK, Glazko GV, Faddeeva NV et al (2004) The effect of mutations altering biogenic amine metabolism in Drosophila on viability and the response to environmental stresses. Arch Insect Biochem Physiol 55:55–67CrossRefPubMedGoogle Scholar
  27. Hiragaki S, Suzuki T, Mohamed AA, Takeda M (2015) Structures and functions of insect arylalkylamine N-acetyltransferase (iaaNAT); a key enzyme for physiological and behavioral switch in arthropods. Front Physiol 6:1–16CrossRefGoogle Scholar
  28. Holden JS, Hadfield JR (1975) Chlordimeform and its effects on monoamine oxidase activity in the cattle tick, Boophilus microplus. Experentia 31:1015–1017CrossRefGoogle Scholar
  29. Hu ZQ, Chen ZZ, Yin ZQ, Jia RY, Song X, Li L, Zou YF, Liang XX, Li LX, He CL, Yin LZ, Lv C et al (2015) In vitro acaricidal activity of 1,8-cineole against Sarcoptes scabiei var. cuniculi and regulating effects on enzyme activity. Parasitol Res 114:2959–2967CrossRefPubMedGoogle Scholar
  30. Isman MB (2006) Botanical insecticides, deterrents, and repellents in modern agricultural and an increasingly regulated world. Annu Rev Entomol 51:45–56CrossRefPubMedGoogle Scholar
  31. Kaufman R, Sloley D (1996) Catabolism of dopamine and 5-hydroxytryptamine by monoamine oxidase in the ixodid tick, Amblyomma hebraeum. Insect Biochem Mol Biol 26:101–109CrossRefPubMedGoogle Scholar
  32. Khajehali J, Van Leeuwen T, Grispou M, Morou E, Alout H, Weill M, Tirry L, Vontasc J, Tsagkarakou A (2010) Acetylcholinesterase point mutations in European strains of Tetranychus urticae (Acari: Tetranychidae) resistant to organophosphates. Pest Manag Sci 66:220–228PubMedGoogle Scholar
  33. Khater HF, Seddiek SA, El-Shorbagy MM, Ali AM (2013) The acaricidal efficacy of peracetic acid and deltamethrin against the fowl tick, Argas persicus, infesting laying hens. Parasitol Res 112:3669–3678CrossRefPubMedGoogle Scholar
  34. Kielkiewicz M (1996) Dispersal of Tetranychus cinnabarinus on various tomato cultivars. Entomol Exp Appl 80:254–257CrossRefGoogle Scholar
  35. Kutsukake M, Komatsu A, Yamamoto D, Ishiwa-Chigusa S (2000) A tyramine receptor gene mutation causes a defective olfactory behavior in Drosophila melanogaster. Gene 245:31–42CrossRefPubMedGoogle Scholar
  36. Lee S, Yoo M, Shin D (2015) The identification and quantification of biogenic amines in Korean turbid rice wine, Makgeolli by HPLC with mass spectrometry detection. LWT Food Sci Technol 62:350–356CrossRefGoogle Scholar
  37. Lei J, Leser M, Enan E (2010) Nematicidal activity of two monoterpenoids and SER-2 tyramine receptor of Caenorhabditis elegans. Biochem Pharmacol 79:1062–1071CrossRefPubMedGoogle Scholar
  38. Leoncini I, Le Conte Y, Costagliola G, Plettner E, Toth AL, Wang MW et al (2004) Regulation of behavioral maturation by a primer pheromone produced by adult worker honey bees. P Natl Acad Sci USA 101:17559–17564CrossRefGoogle Scholar
  39. Libersat F, Pfluger HJ (2004) Monoamines and the orchestration of behavior. Bioscience 54:17–25CrossRefGoogle Scholar
  40. López MD, Pascual-Villalobos MJ (2010) Mode of inhibition of acetylcholinesterase by monoterpenoids and implications for pest control. Ind Crop Prod 31:284–288CrossRefGoogle Scholar
  41. Maccioni E, Alcaro S, Orallo F, Cardia MC, Distinto S, Costa G, Yanez M et al (2010) Synthesis of new 3-aryl-4,5-dihydropyrazole-1-carbothioamide derivatives. An investigation on their ability to inhibit monoamine oxidase. Eur J Med Chem 45:4490–4498CrossRefPubMedGoogle Scholar
  42. Malamud JG, Miszin AP, Josephson RK (1988) The effects of octopamine on contraction kinetics and power output of the locust flight muscle. J Comp Physiol 162:827–835CrossRefGoogle Scholar
  43. Marcic D (2012) Acaricides in modern management of plant-feeding mites. J Pest Sci 85:395–408CrossRefGoogle Scholar
  44. Mi AY, Tae SJ, Doo SP, Ming ZX, Hyun WO, Kyoung BS et al (2006) Antioxidant effects of quinoline alkaloids and 2,4-di-tert-butylphenol isolated from Scolopendra subspinipes. Biol Pharm Bull 29:735–739CrossRefGoogle Scholar
  45. Mukherjee PK, Kumar V, Mal M, Houghton PJ (2007) Acetylcholinesterase inhibitors from plants. Phytomedicine 14:289–300CrossRefPubMedGoogle Scholar
  46. Pophof B (2002) Octopamine enhances moth olfactory responses to pheromones, but not those to general odorants. J Comp Physiol A 188:659–662CrossRefGoogle Scholar
  47. Roeder T (2002) Biochemistry and molecular biology of receptors for biogenic amines in locusts. Microsc Res Tech 56:237–247CrossRefPubMedGoogle Scholar
  48. Roeder T (2005) Tyramine and octopamine: ruling behavior and metabolism. Annu Rev Entomol 50:447–477CrossRefPubMedGoogle Scholar
  49. Saidemberg DM, Ferreira MAB, Takahashi TN, Gomes PC, Cesar-Tognoli LMM et al (2009) Monoamine oxidase inhibitory activities of indolylalkaloid toxins from the venom of the colonial spider Parawixia bistriata: functional characterization of PwTX-I. Toxicon 54:717–724CrossRefPubMedGoogle Scholar
  50. Salgado VL (1998) Studies on the mode of action of spinosad: insect symptoms and physiological correlates. Pestic Biochem Physiol 60:91–102CrossRefGoogle Scholar
  51. Sang MK, Kim JD, Kim BS, Kim KD (2011) Root treatment with rhizobacteria antagonistic to phytophthora blight affects anthracnose occurrence, ripening, and yield of pepper fruit in the plastic house and field. Phytopathology 101:666–678CrossRefPubMedGoogle Scholar
  52. SAS Institute (2002) SAS OnlineDoc®, Version 9.2. Statistical Analysis System Institute. Cary, North Carolina, USAGoogle Scholar
  53. Shih JC, Chen K, Ridd MJ (1999) Monoamine oxidase: from genes to behavior. Annu Rev Neurosci 22:197–217CrossRefPubMedPubMedCentralGoogle Scholar
  54. Stumpf N, Zebitz CPW, Kraus W, Moores GD, Nauen R (2001) Resistance to organophosphates and biochemical genotyping of acetylcholinesterases in Tetranychus urticae (Acari: Tetranychidae). Pestic Biochem Physiol 69:131–142CrossRefGoogle Scholar
  55. Thamm M, Rolke D, Jordan N, Balfanz S, Schiffer C, Baumann A, Blenau W (2013) Function and distribution of 5-HT2 receptors in the honeybee (Apis mellifera). PLoS ONE 8:e82407CrossRefPubMedPubMedCentralGoogle Scholar
  56. Thomas JC, Adams DG, Nessler CL, Brown JK, Bohnert HJ (1995) Tryptophan decarboxylase, tryptamine, and reproduction of the whitefly. Plant Physiol 109:717–720CrossRefPubMedPubMedCentralGoogle Scholar
  57. Thomas JC, Saleh EF, Alammar N, Akroush AM (1998) The indole alkaloid tryptamine impairs reproduction in Drosophila melanogaster. J Econ Entomol 91:841–846CrossRefPubMedGoogle Scholar
  58. Tong F, Coats JR (2012) Quantitative structure-activity relationships of monoterpenoid binding activities to the housefly GABA receptor. Pest Manag Sci 68:1122–1129CrossRefPubMedGoogle Scholar
  59. Tongpoothorn W, Chanthai S, Sriuttha M, Saosang K, Ruangviriyachai C (2012) Bioactive properties and chemical constituents of methanolic extract and its fractions from Jatropha curcas oil. Ind Crops Prod 36:437–444CrossRefGoogle Scholar
  60. Tuberoso CIG, Congiu F, Serreli G, Mameli S (2015) Determination of dansylated amino acids and biogenic amines in Cannonau and Vermentino wines by HPLC-FLD. Food Chem 175:29–35CrossRefPubMedGoogle Scholar
  61. Van Leeuwen T, Tirry L, Yamamoto A, Nauen R, Dermauw W (2015) The economic importance of acaricides in the control of phytophagous mites and an update on recent acaricide mode of action research. Pestic Biochem Physiol 121:12–21CrossRefPubMedGoogle Scholar
  62. Wang YN, Jin YS, Bu CY, Cheng J, Zhao LL, Shi GL (2010) Assessment of the contact toxicity of methyl palmitate on Tetranychus viennensis (Acari: Tetranychidae). J Econ Entomol 103:1372–1377CrossRefPubMedGoogle Scholar
  63. Yu SJ (2008) The toxicology and biochemistry of insecticides. Taylor and Francis Inc., PhiladelphiaGoogle Scholar
  64. Zhang LH, Cai HL, Jiang P, Li HD, Cao LJ, Dang RL, Zhu WY, Deng Y (2015) Simultaneous determination of multiple neurotransmitters and their metabolites in rat brain homogenates and microdialysates by LC-MS/MS. Anal Methods 7:3929–3938CrossRefGoogle Scholar
  65. Žižka Z, Pelc R, Jizba J, Kandybin NV, Sergeeva MV (1997) In situ assessment at subcellular level of the effects of macrotetrolide insecticides on mites by electron microscopy and X-ray. Pestic Biochem Physiol 58:165–172CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Yijuan Chen
    • 1
  • Cédric Bertrand
    • 2
  • Guanghui Dai
    • 1
  • Jiaojian Yuan
    • 3
  1. 1.Plant Health and Natural Products Lab, Key Lab of Urban Agriculture (South), Ministry of Agriculture, School of Agriculture and BiologyShanghai Jiao Tong UniversityShanghaiPeople’s Republic of China
  2. 2.CRIOBE USR 3278, Centre de PhytopharmacieUniversité de PerpignanPerpignan CedexFrance
  3. 3.Instrumental Analysis Center of Shanghai Jiao Tong UniversityShanghaiPeople’s Republic of China

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