Advertisement

Chemical composition, Aedes mosquito larvicidal activity, and repellent activity against Triatoma rubrofasciata of Severinia monophylla leaf essential oil

  • Prabodh Satyal
  • Ho Viet Hieu
  • Nguyen Thi Hong Chuong
  • Nguyen Huy HungEmail author
  • Le Hoang Sinh
  • Pham Van The
  • Thieu Anh Tai
  • Vu Thi Hien
  • William N. SetzerEmail author
Arthropods and Medical Entomology - Original Paper

Abstract

Aedes aegypti and Ae. albopictus are key vectors in the spread of arboviruses such as dengue, chikungunya, yellow fever, and Zika. Triatoma rubrofasciata is an “assassin bug” whose populations and association with humans have dramatically increased and may represent a serious health concern. Control of insect vectors is a logical course of action to prevent the spread of these insect-borne infections. This work presents the leaf essential oil composition, mosquito larvicidal activities, and insect-repellent activity of Severinia monophylla. The essential oil of S. monophylla from Vietnam was obtained by hydrodistillation and analyzed by gas chromatography and mass spectrometry. The major components were sabinene, β-caryophyllene, bicyclogermacrene, germacrene D, (E)-nerolidol, globulol, and linalool. The leaf essential oil showed remarkable larvicidal activity against Ae. aegypti with LC50 (48 h) of 7.1 μg/mL and Ae. albopictus with LC50 (48 h) of 36 μg/mL. The essential oil also showed repellent activity on T. rubrofasciata at a concentration of 0.5%.

Keywords

Dengue fever Trypanosomiasis Sabinene β-Caryophyllene Vector control Vietnam 

Notes

Acknowledgments

The authors are grateful to Duy Tan University for financial support of this research project. P.S. and W.N.S. participated in this work as part of the activities of the Aromatic Plant Research Center (APRC, https://aromaticplant.org/); we are grateful to dōTERRA International (https://www.doterra.com/US/en) for the financial support of the APRC.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Abou-Taleb HK, Mohamed MIE, Shawir MS, Abdelgaleil SAM (2016) Insecticidal properties of essential oils against Tribolium castaneum (Herbst) and their inhibitory effects on acetylcholinesterase and adenosine triphosphatases. Nat Prod Res 30:710–714.  https://doi.org/10.1080/14786419.2015.1038999 CrossRefGoogle Scholar
  2. Adams RP (2007) Identification of essential oil components by gas chromatography/mass spectrometry, 4th edn. Allured Publishing, Carol StreamGoogle Scholar
  3. Airy-Shaw HK (1939) Notes on the nomenclature of certain Rutaceae-Aurantioideae. Bull Misc Inf (Royal Bot Gard Kew) 1939:290–293Google Scholar
  4. Barrett ADT, Higgs S (2007) Yellow fever: a disease that has yet to be conquered. Annu Rev Entomol 52:209–229.  https://doi.org/10.1146/annurev.ento.52.110405.091454 CrossRefGoogle Scholar
  5. Baskar K, Sudha V, Nattudurai G, Ignacimuthu S, Duraipandiyan V, Jayakumar M, al-Dhabi NA, Benelli G (2018) Larvicidal and repellent activity of the essential oil from Atalantia monophylla on three mosquito vectors of public health importance, with limited impact on non-target zebra fish. Physiol Mol Plant Pathol 101:197–201.  https://doi.org/10.1016/j.pmpp.2017.03.002 CrossRefGoogle Scholar
  6. Benelli G (2015) Research in mosquito control: current challenges for a brighter future. Parasitol Res 114:2801–2805.  https://doi.org/10.1007/s00436-015-4586-9 CrossRefGoogle Scholar
  7. Benelli G, Mehlhorn H (2016) Declining malaria, rising of dengue and Zika virus: insights for mosquito vector control. Parasitol Res 115:1747–1754.  https://doi.org/10.1007/s00436-016-4971-z CrossRefGoogle Scholar
  8. Benelli G, Pavela R (2018) Beyond mosquitoes—essential oil toxicity and repellency against bloodsucking insects. Ind Crop Prod 117:382–392.  https://doi.org/10.1016/j.indcrop.2018.02.072 CrossRefGoogle Scholar
  9. Benelli G, Flamini G, Canale A et al (2012) Repellence of Hyptis suaveolens whole essential oil and major constituents against adults of the granary weevil Sitophilus granarius. Bull Insectol 65:177–183Google Scholar
  10. Benelli G, Pavela R, Lupidi G, Nabissi M, Petrelli R, Ngahang Kamte SL, Cappellacci L, Fiorini D, Sut S, Dall’Acqua S, Maggi F (2018) The crop-residue of fiber hemp cv. Futura 75: from a waste product to a source of botanical insecticides. Environ Sci Pollut Res 25:10515–10525.  https://doi.org/10.1007/s11356-017-0635-5 CrossRefGoogle Scholar
  11. Bonesi M, Menichini F, Tundis R, Loizzo MR, Conforti F, Passalacqua NG, Statti GA, Menichini F (2010) Acetylcholinesterase and butyrylcholinesterase inhibitory activity of Pinus species essential oils and their constituents. J Enzyme Inhib Med Chem 25:622–628.  https://doi.org/10.3109/14756360903389856 CrossRefGoogle Scholar
  12. Brummitt RK (1998) Report of the committee for spermatophyta: 46. Taxon 1998:441–444CrossRefGoogle Scholar
  13. Casida JE, Quistad GB (2000) Insecticide targets: learning to keep up with resistance and changing concepts of safety. Agric Chem Biotechnol 43:185–191Google Scholar
  14. Cheng SS, Lin CY, Chung MJ, Liu YH, Huang CG, Chang ST (2013) Larvicidal activities of wood and leaf essential oils and ethanolic extracts from Cunninghamia konishii Hayata against the dengue mosquitoes. Ind Crop Prod 47:310–315.  https://doi.org/10.1016/j.indcrop.2013.03.016 CrossRefGoogle Scholar
  15. Claver MA, Yaqub A (2015) Morphometric analysis of tropicopolitan bug Triatoma rubrofasciata (De Geer) in two different parts of India. Int J Res Stud Biosci 3:130–138Google Scholar
  16. Dambolena JS, Zunino MP, Herrera JM et al (2016) Terpenes: natural products for controlling insects of importance to human health - a structure-activity relationship study. Psyche (New York) 2016:4595823.  https://doi.org/10.1155/2016/4595823 Google Scholar
  17. Das AK, Swamy PS (2013) Comparison of the volatile oil composition of three Atalantia species. J Environ Biol 34:569–571Google Scholar
  18. Das AK, Suresh Kumar J, Swamy PS (2015) Larvicidal activity and leaf essential oil composition of three species of genus Atalantia from south India. Int J Mosq Res 2:25–29Google Scholar
  19. Dekker T, Ignell R, Ghebru M, Glinwood R, Hopkins R (2011) Identification of mosquito repellent odours from Ocimum forskolei. Parasit Vectors 4:183.  https://doi.org/10.1186/1756-3305-4-183 CrossRefGoogle Scholar
  20. Dhimal M, Gautam I, Joshi HD, Hara RBO (2015) Risk factors for the presence of Chikungunya and dengue vectors (Aedes aegypti and Aedes albopictus), their altitudinal distribution and climatic determinants of their abundance in central Nepal. PLoS Negl Trop Dis 9:e0003545.  https://doi.org/10.1371/journal.pntd.0003545 CrossRefGoogle Scholar
  21. Dias CN, Fernandes D, Moraes C (2014) Essential oils and their compounds as Aedes aegypti L. (Diptera: Culicidae) larvicide: review. Parasitol Res 113:565–592.  https://doi.org/10.1007/s00436-013-3687-6 CrossRefGoogle Scholar
  22. Do TL (2004) Medicinal plants and drugs from Vietnam. Medical Publishing House, HanoiGoogle Scholar
  23. Dohi S, Terasaki M, Makino M (2009) Acetylcholinesterase inhibitory activity and chemical composition of commercial essential oils. J Agric Food Chem 57:4313–4318.  https://doi.org/10.1021/jf804013j CrossRefGoogle Scholar
  24. Duc T, Quynh LTN, Nghi NP et al (2008) Research on chemical composition and biological activity of Severina monophylla leaf. J Sci Technol Univ Da Nang 6:71–76Google Scholar
  25. Dujardin JP, Lam TX, Khoa PT, Schofield CJ (2015) The rising importance of Triatoma rubrofasciata. Mem Inst Oswaldo Cruz 110:319–323.  https://doi.org/10.1590/0074-02760140446 CrossRefGoogle Scholar
  26. Enan E (2001) Insecticidal activity of essential oils: octopaminergic sites of action. Comp Biochem Physiol - C Toxicol Pharmacol 130:325–337.  https://doi.org/10.1016/S1532-0456(01)00255-1 CrossRefGoogle Scholar
  27. Enan EE (2005) Molecular and pharmacological analysis of an octopamine receptor from American cockroach and fruit fly in response to plant essential oils. Arch Insect Biochem Physiol 59:161–171.  https://doi.org/10.1002/arch.20076 CrossRefGoogle Scholar
  28. Ferrero AA, Werdin González JO, Sánchez Chopa C (2006) Biological activity of Schinus molle on Triatoma infestans. Fitoterapia 77:381–383.  https://doi.org/10.1016/j.fitote.2006.03.004 CrossRefGoogle Scholar
  29. ffrench-Constant RH, Williamson MS, Davies TGE, Bass C (2016) Ion channels as insecticide targets. J Neurogenet 30:163–177.  https://doi.org/10.1080/01677063.2016.1229781 CrossRefGoogle Scholar
  30. Finney D (2009) Probit analysis, Reissue Ed. Cambridge University Press, CambridgeGoogle Scholar
  31. Giatropoulos A, Pitarokili D, Papaioannou F, Papachristos DP, Koliopoulos G, Emmanouel N, Tzakou O, Michaelakis A (2013) Essential oil composition, adult repellency and larvicidal activity of eight Cupressaceae species from Greece against Aedes albopictus (Diptera: Culicidae). Parasitol Res 112:1113–1123.  https://doi.org/10.1007/s00436-012-3239-5 CrossRefGoogle Scholar
  32. Gómez A, Seccacini E, Zerba E, Licastro S (2011) Comparison of the insecticide susceptibilities of laboratory strains of Aedes aegypti and Aedes albopictus. Mem Inst Oswaldo Cruz 106:993–996.  https://doi.org/10.1590/S0074-02762011000800015 CrossRefGoogle Scholar
  33. Goulson D (2013) An overview of the environmental risks posed by neonicotinoid insecticides. J Appl Ecol 50:977–987.  https://doi.org/10.1111/1365-2664.12111 CrossRefGoogle Scholar
  34. Govindarajan M, Rajeswary M, Hoti SL, Bhattacharyya A, Benelli G (2016) Eugenol, α-pinene and β-caryophyllene from Plectranthus barbatus essential oil as eco-friendly larvicides against malaria, dengue and Japanese encephalitis mosquito vectors. Parasitol Res 115:807–815.  https://doi.org/10.1007/s00436-015-4809-0 CrossRefGoogle Scholar
  35. Gross AD, Kimber MJ, Day TA et al (2013) Quantitative structure-activity relationships (QSARs) of monoterpenoids at an expressed American cockroach octopamine receptor. ACS Symp Ser 1141:97–110.  https://doi.org/10.1021/bk-2013-1141.ch007 CrossRefGoogle Scholar
  36. Gubler DJ (1998) Dengue and dengue hemorrhagic fever. Clin Microbiol Rev 11:480–496CrossRefGoogle Scholar
  37. Hemingway J, Ranson H (2000) Insecticide resistance in insect vectors of human disease. Annu Rev Entomol 45:371–391CrossRefGoogle Scholar
  38. Hijaz F, Nehela Y, Killiny N (2016) Possible role of plant volatiles in tolerance against huanglongbing in citrus. Plant Signal Behav 11:1–12.  https://doi.org/10.1080/15592324.2016.1138193 Google Scholar
  39. Jankowska M, Rogalska J, Wyszkowska J, Stankiewicz M (2018) Molecular targets for components of essential oils in the insect nervous system - a review. Molecules 23:34.  https://doi.org/10.3390/molecules23010034 CrossRefGoogle Scholar
  40. Kamrin MA (1997) Pesticide profiles: toxicity, environmental impact, and fate. CRC Press, Boca RatonCrossRefGoogle Scholar
  41. Kang JS, Kim E, Lee SH, Park I-K (2013) Inhibition of acetylcholinesterases of the pinewood nematode, Bursaphelenchus xylophilus, by phytochemicals from plant essential oils. Pestic Biochem Physiol 105:50–56.  https://doi.org/10.1016/j.pestbp.2012.11.007 CrossRefGoogle Scholar
  42. Karatolos N, Pauchet Y, Wilkinson P, Chauhan R, Denholm I, Gorman K, Nelson DR, Bass C, ffrench-Constant RH, Williamson MS (2011) Pyrosequencing the transcriptome of the greenhouse whitefly, Trialeurodes vaporariorum reveals multiple transcripts encoding insecticide targets and detoxifying enzymes. BMC Genomics 12:56.  https://doi.org/10.1186/1471-2164-12-56 CrossRefGoogle Scholar
  43. Koutsaviti K, Giatropoulos A, Pitarokili D, Papachristos D, Michaelakis A, Tzakou O (2014) Greek Pinus essential oils: larvicidal activity and repellency against Aedes albopictus (Diptera: Culicidae). Parasitol Res 114:583–592.  https://doi.org/10.1007/s00436-014-4220-2 CrossRefGoogle Scholar
  44. Lanteigne M, Whiting SA, Lydy MJ (2015) Mixture toxicity of imidacloprid and cyfluthrin to two non-target species, the fathead minnow Pimephales promelas and the amphipod Hyalella azteca. Arch Environ Contam Toxicol 68:354–361.  https://doi.org/10.1007/s00244-014-0086-7 CrossRefGoogle Scholar
  45. Lardeux F, Depickère S, Duchon S, Chavez T (2010) Insecticide resistance of Triatoma infestans (Hemiptera, Reduviidae) vector of Chagas disease in Bolivia. Trop Med Int Heal 15:1037–1048.  https://doi.org/10.1111/j.1365-3156.2010.02573.x Google Scholar
  46. Laurent D, Vilaseca LA, Chanttraine J-M et al (1997) Insecticidal activity of essential oils on Triatoma infestans. Phyther Res 11:285–290CrossRefGoogle Scholar
  47. Le Quyen D, Le NT, Van Anh CT et al (2018) Epidemiological, serological, and virological features of dengue in Nha Trang City, Vietnam. Am J Trop Med Hyg 98:402–409.  https://doi.org/10.4269/ajtmh.17-0630 CrossRefGoogle Scholar
  48. Leal-Cardoso JH, da Silva-Alves KS, Ferreira-da-Silva FW, dos Santos-Nascimento T, Joca HC, de Macedo FHP, de Albuquerque-Neto PM, Magalhães PJC, Lahlou S, Cruz JS, Barbosa R (2010) Linalool blocks excitability in peripheral nerves and voltage-dependent Na+ current in dissociated dorsal root ganglia neurons. Eur J Pharmacol 645:86–93.  https://doi.org/10.1016/j.ejphar.2010.07.014 CrossRefGoogle Scholar
  49. Lima B, López S, Luna L, Agüero MB, Aragón L, Tapia A, Zacchino S, López ML, Zygadlo J, Feresin GE (2011) Essential oils of medicinal plants from the central Andes of Argentina: chemical composition, and antifungal, antibacterial, and insect-repellent activities. Chem Biodivers 8:924–936CrossRefGoogle Scholar
  50. Liu N (2015) Insecticide resistance in mosquitoes: impact, mechanisms, and research directions. Annu Rev Entomol 60:537–559.  https://doi.org/10.1146/annurev-ento-010814-020828 CrossRefGoogle Scholar
  51. López MD, Pascual-Villalobos MJ (2010) Mode of inhibition of acetylcholinesterase by monoterpenoids and implications for pest control. Ind Crop Prod 31:284–288.  https://doi.org/10.1016/j.indcrop.2009.11.005 CrossRefGoogle Scholar
  52. López SB, López ML, Aragón LM et al (2011) Composition and anti-insect activity of essential oils from Tagetes L species (Asteraceae, Helenieae) on Ceratitis capitata Wiedemann and Triatoma infestans Klug. J Agric Food Chem 59:5286–5292.  https://doi.org/10.1021/jf104966b CrossRefGoogle Scholar
  53. Masetti A (2016) The potential use of essential oils against mosquito larvae: a short review. Bull Insectol 69:307–310Google Scholar
  54. Menichini F, Tundis R, Loizzo MR, Bonesi M, Marrelli M, Statti GA, Menichini F, Conforti F (2009) Acetylcholinesterase and butyrylcholinesterase inhibition of ethanolic extract and monoterpenes from Pimpinella anisoides V Brig. (Apiaceae). Fitoterapia 80:297–300.  https://doi.org/10.1016/j.fitote.2009.03.008 CrossRefGoogle Scholar
  55. Missouri Botanical Garden (2018) Tropicos.org. In: Tropicos.org. www.tropicos.org. Accessed 27 Jul 2018
  56. Mougabure-Cueto G, Picollo MI (2015) Insecticide resistance in vector Chagas disease: evolution, mechanisms and management. Acta Trop 149:70–85.  https://doi.org/10.1016/j.actatropica.2015.05.014 CrossRefGoogle Scholar
  57. Nair KN, Barrie FR (1995) (1168) Proposal to change the listed type of Atalantia Corrêa (Rutaceae), nom. cons. Taxon 1995:429–432CrossRefGoogle Scholar
  58. Naqqash MN, Gökçe A, Bakhsh A, Salim M (2016) Insecticide resistance and its molecular basis in urban insect pests. Parasitol Res 115:1363–1373.  https://doi.org/10.1007/s00436-015-4898-9 CrossRefGoogle Scholar
  59. Narusuye K, Kawai F, Matsuzaki K, Miyachi E (2005) Linalool suppresses voltage-gated currents in sensory neurons and cerebellar Purkinje cells. J Neural Transm 112:193–203.  https://doi.org/10.1007/s00702-004-0187-y CrossRefGoogle Scholar
  60. Nattudurai G, Baskar K, Paulraj MG, Islam VIH, Ignacimuthu S, Duraipandiyan V (2017) Toxic effect of Atalantia monophylla essential oil on Callosobruchus maculatus and Sitophilus oryzae. Environ Sci Pollut Res 24:1619–1629.  https://doi.org/10.1007/s11356-016-7857-9 CrossRefGoogle Scholar
  61. Ochocka JR, Asztemborska M, Sybilska D, Langa W (2002) Determination of enantiomers of terpenic hydrocarbons in essential oils obtained from species of Pinus and Abies. Pharm Biol 40:395–399CrossRefGoogle Scholar
  62. Olmedo R, Herrera JM, Lucini EI et al (2015) Essential oil of Tagetes filifolia against the flour beetle Tribolium castaneum and its relation to acetylcholinesterase activity and lipid peroxidation. Agriscientia 32:113–121Google Scholar
  63. Park IK, Lee SG, Choi DH, Park JD, Ahn YJ (2003) Insecticidal activities of constituents identified in the essential oil from leaves of Chamaecyparis obtusa against Callosobruchus chinensis (L.) and Sitophilus oryzae (L.). J Stored Prod Res 39:375–384.  https://doi.org/10.1016/S0022-474X(02)00030-9 CrossRefGoogle Scholar
  64. Patterson JS, Schofield CJ, Dujardin JP, Miles MA (2001) Population morphometric analysis of the tropicopolitan bug Triatoma rubrofasciata and relationships with Old World species of Triatoma: evidence of New World ancestry. Med Vet Entomol 15:443–451.  https://doi.org/10.1046/j.0269-283X.2001.00333.x CrossRefGoogle Scholar
  65. Pavela R (2015) Essential oils for the development of eco-friendly mosquito larvicides: a review. Ind Crop Prod 76:174–187CrossRefGoogle Scholar
  66. Pavela R, Benelli G (2016) Essential oils as ecofriendly biopesticides? Challenges and constraints. Trends Plant Sci 21:1000–1007.  https://doi.org/10.1016/j.tplants.2016.10.005 CrossRefGoogle Scholar
  67. Pavela R, Maggi F, Lupidi G, Mbuntcha H, Woguem V, Womeni HM, Barboni L, Tapondjou LA, Benelli G (2018) Clausena anisata and Dysphania ambrosioides essential oils: from ethno-medicine to modern uses as effective insecticides. Environ Sci Pollut Res 25:10493–10503.  https://doi.org/10.1007/s11356-017-0267-9 CrossRefGoogle Scholar
  68. Pham HH (2002) Cay Co Vietnam - an illustrated flora of Vietnam 2. Tre Publishing House, Ho Chi MinhGoogle Scholar
  69. Pino JA, Marbot R, Fuentes V (2006) Aromatic plants from western Cuba. VI. Composition of the leaf oils of Murraya exotica L., Amyris balsamifera L., Severinia buxifolia (Poir.) Ten. and Triphasia trifolia (Burm. f.) P. Wilson. J Essent Oil Res 18:24–28CrossRefGoogle Scholar
  70. Quyen NTH, Kien DTH, Rabaa M et al (2017) Chikungunya and Zika virus cases detected against a backdrop of endemic dengue transmission in Vietnam. Am J Trop Med Hyg 97:146–150.  https://doi.org/10.4269/ajtmh.16-0979 CrossRefGoogle Scholar
  71. Rattan RS (2010) Mechanism of action of insecticidal secondary metabolites of plant origin. Crop Prot 29:913–920.  https://doi.org/10.1016/j.cropro.2010.05.008 CrossRefGoogle Scholar
  72. Royal Botanic Gardens K (2018) The plant list. http://www.theplantlist.org/. Accessed 27 Jul 2018
  73. Safaa AN, Mostafa AAK, Maha MS, Mohamed SH (2018) The impact of seasonal variation on the volatile oil profile of leaves of Severinia buxifolia (Poir.) and its antimicrobial activity. J Pharmacogn Phyther 10:56–63.  https://doi.org/10.5897/JPP2018.0488 CrossRefGoogle Scholar
  74. Satyal P (2015) Development of GC-MS database of essential oil components by the analysis of natural essential oils and synthetic compounds and discovery of biologically active novel chemotypes in essential oils. Ph.D. dissertation, University of Alabama in HuntsvilleGoogle Scholar
  75. Satyal P, Paudel P, Poudel A, Dosoky NS, Pokharel KK, Setzer WN (2013) Bioactivities and compositional analyses of Cinnamomum essential oils from Nepal: C. camphora, C. tamala, and C. glaucescens. Nat Prod Commun 8:1777–1784Google Scholar
  76. Scalerandi E, Flores GA, Palacio M, Defagó MT, Carpinella MC, Valladares G, Bertoni A, Palacios SM (2018) Understanding synergistic toxicity of terpenes as insecticides: contribution of metabolic detoxification in Musca domestica. Front Plant Sci 9:1579.  https://doi.org/10.3389/fpls.2018.01579 CrossRefGoogle Scholar
  77. Scora RW, Ahmed M (1994) The leaf oils of Severinia buxifolia (Poir.) Tenore. J Essent Oil Res 6:363–367CrossRefGoogle Scholar
  78. Silva WJ, Dória GAA, Maia RT, Nunes RS, Carvalho GA, Blank AF, Alves PB, Marçal RM, Cavalcanti SCH (2008) Effects of essential oils on Aedes aegypti larvae: alternatives to environmentally safe insecticides. Bioresour Technol 99:3251–3255.  https://doi.org/10.1016/j.biortech.2007.05.064 CrossRefGoogle Scholar
  79. Smith LB, Kasai S, Scott JG (2016) Pyrethroid resistance in Aedes aegypti and Aedes albopictus: important mosquito vectors of human diseases. Pestic Biochem Physiol 133:1–12.  https://doi.org/10.1016/j.pestbp.2016.03.005 CrossRefGoogle Scholar
  80. Suchail S, Guez D, Belzunces LP (2000) Characteristics of imidacloprid toxicity in two Apis mellifera subspecies. Environ Toxicol Chem 19:1901.  https://doi.org/10.1897/1551-5028(2000)019<1901:COITIT>2.3.CO;2 CrossRefGoogle Scholar
  81. Sugita N, Agemori H, Goka K (2018) Acute toxicity of neonicotinoids and some insecticides to first instar nymphs of a non-target damselfly, Ischnura senegalensis (Odonata: Coenagrionidae), in Japanese paddy fields. Appl Entomol Zool 53:519–524.  https://doi.org/10.1007/s13355-018-0583-7 CrossRefGoogle Scholar
  82. Tak JH, Isman MB (2017) Penetration-enhancement underlies synergy of plant essential oil terpenoids as insecticides in the cabbage looper, Trichoplusia ni. Sci Rep 7:42432.  https://doi.org/10.1038/srep42432 CrossRefGoogle Scholar
  83. Tanaka T (1931) Notes on the Dutch Indian species of Rutaceae-Aurantieae (Revisio Aurantiacearum - V.). Meded s Rijks Herb Leiden 69:4–18Google Scholar
  84. Thirugnanasampandan R, Gunasekar R, Gogulramnath M (2017) Chemical composition analysis, antioxidant and antibacterial activity evaluation of Atalantia monophylla Correa. Pharm Res 7:S52–S56Google Scholar
  85. Tong F, Coats JR (2012) Quantitative structure-activity relationships of monoterpenoid binding activities to the housefly GABA receptor. Pest Manag Sci 68:1122–1129.  https://doi.org/10.1002/ps.3280 CrossRefGoogle Scholar
  86. Vontas J, Kioulos E, Pavlidi N, Morou E, della Torre A, Ranson H (2012) Insecticide resistance in the major dengue vectors Aedes albopictus and Aedes aegypti. Pestic Biochem Physiol 104:126–131.  https://doi.org/10.1016/j.pestbp.2012.05.008 CrossRefGoogle Scholar
  87. Wheeler GS, Massey LM, Southwell IA (2003) Dietary influences on terpenoids sequestered by the biological control agent Oxyops vitiosa: effect of plant volatiles from different Melaleuca quinquenervia chemotypes and laboratory host species. J Chem Ecol 29:189–208.  https://doi.org/10.1023/a:1021941000399 CrossRefGoogle Scholar
  88. Wunderlin RP (1998) A guide to the vascular plants of Florida. University Press of Florida, GainesvilleGoogle Scholar
  89. Yeom H-J, Jung C-S, Kang J, Kim J, Lee JH, Kim DS, Kim HS, Park PS, Kang KS, Park IK (2015) Insecticidal and acetylcholine esterase inhibition activity of Asteraceae plant essential oils and their constituents against adults of the German cockroach (Blattella germanica). J Agric Food Chem 63:2241–2248.  https://doi.org/10.1021/jf505927n CrossRefGoogle Scholar
  90. Zarrad K, Ben Hamouda A, Chaieb I et al (2015) Chemical composition, fumigant and anti-acetylcholinesterase activity of the Tunisian Citrus aurantium L. essential oils. Ind Crop Prod 76:121–127.  https://doi.org/10.1016/j.indcrop.2015.06.039 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Aromatic Plant Research CenterLehiUSA
  2. 2.Parasitology and Entomology Unit, Department of MedicineDuy Tan UniversityDa NangVietnam
  3. 3.Center for Advanced Chemistry, Institute of Research and DevelopmentDuy Tan UniversityDa NangVietnam
  4. 4.Center of Scientific Research and PracticeThu Dau Mot UniversityThu Dau Mot cityVietnam
  5. 5.Department of PharmacyDuy Tan UniversityDa NangVietnam
  6. 6.Faculty of HydrometerologyHo Chi Minh City University of Natural Resources and EnvironmentHo Chi Minh CityVietnam
  7. 7.Department of ChemistryUniversity of Alabama in HuntsvilleHuntsvilleUSA

Personalised recommendations