Environmental Science and Pollution Research

, Volume 25, Issue 11, pp 10493–10503 | Cite as

Clausena anisata and Dysphania ambrosioides essential oils: from ethno-medicine to modern uses as effective insecticides

  • Roman Pavela
  • Filippo Maggi
  • Giulio Lupidi
  • Hélène Mbuntcha
  • Verlaine Woguem
  • Hilaire Macaire Womeni
  • Luciano Barboni
  • Léon Azefack Tapondjou
  • Giovanni Benelli
Plant-borne compounds and nanoparticles: challenges for medicine, parasitology and entomology

Abstract

Dysphania ambrosioides (L.) Mosyakin & Clemants (Amaranthaceae) and Clausena anisata (Willd.) Hook. f. ex Benth. (Rutaceae) are two aromatic species traditionally used in Cameroon to repel and kill insects. The present work was carried out to substantiate this traditional use and to evaluate the possible incorporation in commercial botanical insecticides of their essential oils (EOs). The EOs were distilled from leaves of C. anisata and aerial parts of D. ambrosioides and analyzed by gas chromatography-mass spectrometry (GC-MS). The insecticidal activity of both EOs was investigated against the filariasis vector, Culex quinquefasciatus, and the housefly, Musca domestica. As possible mode of action, the inhibition of acetylcholinesterase (AChE) by the two EOs was investigated as well. The D. ambrosioides EO was characterized by the monoterpene peroxide ascaridole (61.4%) and the aromatic p-cymene (29.0%), whereas the C. anisata EO was dominated by the phenylpropanoids (E)-anethole (64.6%) and (E)-methyl isoeugenol (16.1%). The C. anisata EO proved to be very toxic to third instar larvae of C. quinquefasciatus showing LC50 of 29.3 μl/l, whereas D. ambrosioides EO was more toxic to adults of M. domestica showing a LD50 of 51.7 μg/adult. The mixture of both EOs showed a significant synergistic effect against mosquito larvae with LC50 estimated as 19.3 μl/l, whereas this phenomenon was not observed upon application to M. domestica adults (LD50 = 75.9 μg/adult). Of the two EOs, the D. ambrosioides one provided a good inhibition of AChE (IC50 = 77 μg/ml), whereas C. anisata oil was not effective. These findings provide new evidences supporting the ethno-botanical use of these two Cameroonian plants, and their possible application even in synergistic binary blends, to develop new eco-friendly, safe and effective herbal insecticides.

Keywords

Culex quinquefasciatus Ethno-botanical pesticides Musca domestica St. Louis encephalitis Dysphania ambrosioides Clausena anisata 

Notes

Acknowledgments

Roman Pavela would like to thank the Ministry of Agriculture of the Czech Republic for its financial support concerning botanical pesticide and basic substances research (Project No. RO0417). Filippo Maggi is grateful to the University of Camerino (Fondo di Ateneo per la Ricerca, FAR 2014/2015, FPI 000044) for financial support.

Author contributions

The contributions of the respective authors are as follows: R. Pavela (pavela@vurv.cz) performed the insecticidal experiments; F. Maggi (filippo.maggi@unicam.it) interpreted data and drafted the manuscript; G. Lupidi (giulio.lupidi@unicam.it) determined the anti-AChE and antioxidant activity; H. Mbuntcha (helenembuntcha@yahoo.fr), V. Woguem (woverly91@yahoo.fr) and H.M. Womeni (womeni@yahoo.fr) collected the plant material and hydrodistilled the EOs; L. Barboni (luciano.barboni@unicam.it) performed the chemical analyses; L.A. Tapondjou (tapondjou2001@yahoo.fr) collected ethno-botanical information and drafted the manuscript; G. Benelli (benelli.giovanni@gmail.com) conceived the research, interpreted and analyzed the data, drafted and revised the manuscript. All authors read and approved the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Abbott WS (1925) A method of computing the effectiveness of an insecticide. J Econ Entomol 18:265–267CrossRefGoogle Scholar
  2. Adams RP (2007) Identification of EO components by gas chromatography/mass spectrometry. 4th edn. Allured, Carol Stream, ILGoogle Scholar
  3. Addae-Mensah I, Asomaning WA, Oteng-Yeboah A, Garneau F-X, Gagnon H, Jean F-I, Moudachirou M, Koumaglo KH (1996) (E)-Anethole as a major EO constituent of Clausena anisata. J Essent Oil Res 8:513–516CrossRefGoogle Scholar
  4. Afshar FH, Maggi F, Iannarelli R, Cianfaglione K, Isman MB (2017) Comparative toxicity of Helosciadium nodiflorum EOs and combinations of their main constituents against the cabbage looper, Trichoplusia ni (Lepidoptera). Ind Crop Prod 98:46–52CrossRefGoogle Scholar
  5. Alitonou GA, Sessou P, Tchobo FP, Noudogbessi JP, Avlessi F, Yehouenou B, Menut C, Villeneuve P, Sohounhloue DCK (2012) Chemical composition and biological activities of EOs of C. ambrosioides L. collected in two areas of Benin. Int J Biosci 8:58–66Google Scholar
  6. Al-kaf AG, Crouch RA, Denkert A, Porzel A, Al-Hawshabi OSS, Ali NAA, Setzer WN, Wessjohann L (2016) Chemical composition and biological activity of EO of Chenopodium ambrosioides from Yemen. Am J EOs Nat Prod 4:20–22Google Scholar
  7. Benelli G (2015a) Research in mosquito control: current challenges for a brighter future. Parasitol Res 114:2801–2805CrossRefGoogle Scholar
  8. Benelli G (2015b) Plant-borne ovicides in the fight against mosquito vectors of medical and veterinary importance: a systematic review. Parasitol Res 114:3201–3212CrossRefGoogle Scholar
  9. Benelli G, Beier J (2017) Current vector control challenges in the fight against malaria. Acta Trop 174:91–96CrossRefGoogle Scholar
  10. Benelli G, Mehlhorn H (2016) Declining malaria, rising dengue and Zika virus: insights for mosquito vector control. Parasitol Res 115:1747–1754CrossRefGoogle Scholar
  11. Benelli G, Romano D (2017) Mosquito vectors of Zika virus. Entomol Gen.  https://doi.org/10.1127/entomologia/2017/0496
  12. Benelli G, Lo Iacono A, Canale A, Mehlhorn H (2016) Mosquito vectors and the spread of cancer: an overlooked connection? Parasitol Res 115:2131–2137CrossRefGoogle Scholar
  13. Benelli G, Pavela R, Iannarelli R, Petrelli R, Cappellacci L, Cianfaglione K, Afshar FH, Nicoletti M, Canale A, Maggi F (2017a) Synergized mixtures of Apiaceae EOs and related plant-borne compounds: larvicidal effectiveness on the filariasis vector Culex quinquefasciatus Say. Ind Crop Prod 96:186–195CrossRefGoogle Scholar
  14. Benelli G, Pavela R, Maggi F, Petrelli R, Nicoletti M (2017b) Commentary: Making green pesticides greener? The potential of plant products for nanosynthesis and pest control. J Clust Sci 28:3–10CrossRefGoogle Scholar
  15. Benelli G, Rajeswary M, Govindarajan M (2017c) Towards green oviposition deterrents? Effectiveness of Syzygium lanceolatum (Myrtaceae) EO against six mosquito vectors and impact on four aquatic biological control agents. Environ Sci Poll Res.  https://doi.org/10.1007/s11356-016-8146-3
  16. Brahim MAS, Fadli M, Hassani L, Boulay B, Markouk M, Bekkouche K, Abbad A, Ali MA, Larhsini M (2015) Chenopodium ambrosioides var. ambrosioides used in Moroccan traditional medicine can enhance the antimicrobial activity of conventional antibiotics. Ind Crop Prod 71:37–43CrossRefGoogle Scholar
  17. Cavalli JF, Tomi F, Bernardini AF, Casanova J (2004) Analysis of the EO of Chenopodium ambrosioides by GC, GC–MS and 13C-NMR spectroscopy: quantitative determination of ascaridole, a heat-sensitive compound. Phytochem Anal 15:275–279CrossRefGoogle Scholar
  18. Chekem MSG, Lunga PK, Tamokou JDD, Kuiate R, Tane P, Vilarem G, Cerny M (2010) Antifungal properties of Chenopodium ambrosioides EO against Candida species. Pharmaceuticals 3:2900–2909CrossRefGoogle Scholar
  19. Chu SS, Hu JF, Liu ZL (2010) Composition of EO of Chinese Chenopodium ambrosioides and insecticidal activity against maize weevil, Sitophilus zeamais. Pest Manag Sci 67:714–718CrossRefGoogle Scholar
  20. de Castro DSB, da Silva DB, Tibúrcio JD, Sobral MEG, Ferraz V, Taranto AG, Serrão JE, de Siqueira JM, Alves SN (2016) Larvicidal activity of EO of Peumus boldus Molina and its ascaridole-enriched fraction against Culex quinquefasciatus. Exp Parasitol 171:84–90CrossRefGoogle Scholar
  21. Dembitsky V, Shkrob I, Hanus LO (2008) Ascaridole and related peroxides from the genus Chenopodium. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub 152:209–215CrossRefGoogle Scholar
  22. Denloye A, Makanjuola W, Teslim O, Alafia O, Kasali A, Eshilokun A (2010) Toxicity of Chenopodium ambrosioides L. (Chenopodiaceae) products from Nigeria against three storage insects. J Plant Prot Res 50(3):379–384CrossRefGoogle Scholar
  23. Ekundayo O, Oguntimein BO, Hammerschmidt FJ (1986) Constituents of the EO of Clausena anisata leaves. Planta Med 6:505–506CrossRefGoogle Scholar
  24. FFNSC 2 (2012) Flavors and fragrances of natural and synthetic compounds. Mass spectral database, Shimadzu Corps, KyotoGoogle Scholar
  25. Finney DJ (1971) Probit analysis. Cambridge University Press, LondonGoogle Scholar
  26. Garneau F-X, Pichette A, Gagnon H, Jean F-I, Addae-Mensah I, Osei-Safu D, Asomaning WA, Oteng-Yeboah A (2000) (E)- and (Z)-Foeniculin, constituents of the leaf oil of a new chemovariety of Clausena anisata. J Essent Oil Res 12:757–762CrossRefGoogle Scholar
  27. Govindarajan M (2010) Chemical composition and larvicidal activity of leaf EO from Clausena anisata (Willd.) Hook. f. ex Benth (Rutaceae) against three mosquito species. Asian Pac J Trop Med 3:874–877CrossRefGoogle Scholar
  28. Guenther E (1960) The EOs, vol I. van Nostrand Company Inc., New York, 372 ppGoogle Scholar
  29. Gundidza M, Chinyanganya F, Chagonda L, Depooter HL, Mavi S (1994) Phytoconstituents and antimicrobial activity of the leaf EO of Clausena anisata (Wild.) J.D. Hook ex. Benth. Flavour Fragr J 9:299–303CrossRefGoogle Scholar
  30. Hamza OJ, van den Bout-van CJ, Matee MI, Moshi MJ, Mikx FH, Selemani HO et al (2006) Antifungal activity of some Tanzanian plants used traditionally for the treatment of fungal infections. J Ethnopharmacol 108(1):124–132CrossRefGoogle Scholar
  31. Hatzakis E, Opsenica I, Solaja BA, Stratakis M (2007) Synthesis of novel polar derivatives of the antimalarial endoperoxides ascaridole and dihydroascaridole. ARKIVOC 8:124–135Google Scholar
  32. Innocent E, Hassanali A (2015) Constituents of EOs from three plant species used in traditional medicine and insect control in Tanzania. J Herbs Spices Med Plants 21:219–229CrossRefGoogle Scholar
  33. Ismail AA, Looi CY, Ahmad BA, Cheah FK, Wong WF, Sukari MA et al (2012) Dentatin Induces Apoptosis in Prostate Cancer Cells via Bcl-2, Bcl-xL, Survivin Downregulation, Caspase-9,-3/7 Activation, and NF-[kappa] B Inhibition. Evidence-Based Compl Altern Med Article ID 856029,  https://doi.org/10.1155/2012/856029
  34. Isman MB (2006) Botanical insecticides, deterrents, and repellents in modern agriculture and an increasingly regulated world. Annu Rev Entomol 51:45–66CrossRefGoogle Scholar
  35. Isman MB, Machial CM (2006) Chapter 2 pesticides based on plant essential oils: from traditional practice to commercialization. Adv Phytomed 3:29–44CrossRefGoogle Scholar
  36. Jardim CM, Jham GN, Dhingra OD, Freire MM (2008) Composition and antifungal activity of the EO of the Brazilian Chenopodium ambrosioides L. J Chem Ecol 34:1213–1218CrossRefGoogle Scholar
  37. Johnson MA, Croteau R (1984) Biosynthesis of ascaridole: iodide peroxidase-catalysed synthesis of a monoterpene endoperoxide in soluble extracts of Chenopodium ambrosioides fruit. Arch Biochem Biophys 235:254–266CrossRefGoogle Scholar
  38. Kenechukwu FC, Mbah CJ, Momoh MA, Chime SA, Umeyor CE, Ogbonna JDN (2012) Pharmacological justification for the ethnomedical use of Clausena anisata root-bark extract in the management of epilepsy. J Applied Pharm Sci http://imsear.li.mahidol.ac.th/handle/123456789/151383
  39. Kishore N, Chansouria JPN, Dubey NK (1996) Antidermatophytic action of the essential oil of Chenopodium ambrosioides and an ointment prepared from it. Phytother Res 10:453–455CrossRefGoogle Scholar
  40. Kumar R, Mishra AK, Dubey NK (2007) Evaluation of Chenopodium ambrosioides oil as a potential source of antifungal, antiaflatoxigenic and antioxidant activity. Int J Food Microbiol 115:159–164CrossRefGoogle Scholar
  41. Makirita W, Chauka L, Chacha M (2015) Larvicidal activity of Clausena anisata fruits and leaves extracts against Anopheles gambiae Giless., Culex quinquefasciatus Say and Aedes egyptiae. SpatulaDD 5:147–153CrossRefGoogle Scholar
  42. Massebo F, Tadesse M, Bekele T, Balkew M, Gebre-Michael T (2009) Evaluation on larvicidal effects of EOs of some local plants against Anopheles arabiensis Patton and Aedes aegypti Linnaeus (Diptera, Culicidae) in Ethiopia. Afr J Biotechnol 8:4183–4188Google Scholar
  43. Moshi MJ, Kagashe GAB, Mbwambo ZH (2005) Plants used to treat epilepsy by Tanzanian traditional healers. J Ethnopharmacol 97:327–336CrossRefGoogle Scholar
  44. Muhayimana A, Chalchat JC, Garry RP (1998) Chemical composition of EOs of Chenopodium ambrosioides L. from Rwanda. J Essent Oil Res 10:690–692CrossRefGoogle Scholar
  45. Naqqash MN, Gökçe A, Bakhsh A, Salim M (2016) Insecticide resistance and its molecular basis in urban insect pests. Parasitol Res 115:1363–1373CrossRefGoogle Scholar
  46. Ndomo AF, Ngamo LT, Tapondjou LA, Tchouanguep FM, Hance T (2008) Insecticidal effects of the powdery formulation based on clay and EO from the leaves of Clausena anisata (Willd.) J. D. Hook ex. Benth. (Rutaceae) against Acanthoscelides obtectus (Say) (Coleoptera: Bruchidae). J Pest Sci 81:227–234CrossRefGoogle Scholar
  47. Ngassoum MB, Jirovetz L, Buchbauer G, Schmaus G, Hammerschmidt F-S (1999) Chemical composition and olfactory evaluation of the EOs of leaves and seeds of Clausena anisata (Willd.) J.D. Hook. ex. Benth. Cameroon. J Essent Oil Res 11:231–237CrossRefGoogle Scholar
  48. NIST 08 (2008) National Institute of Standards and Technology Mass Spectral Library (NIST/EPA/NIH). National Institute of Standards and Technology, Gaithersburg, MDGoogle Scholar
  49. Okokon JE, Etebong EO, Udobang JA, Essien GE (2012) Antiplasmodial and analgesic activities of Clausena anisata. Asian Pacific J Trop Med 5(3):214–219CrossRefGoogle Scholar
  50. Okunade AL, Olaifa JI (1987) Estragole: an acute toxic principle of the leaves of Clausena anisata. J Nat Prod 50:990–991CrossRefGoogle Scholar
  51. Ole-Miaron JO (2003) The Maasai ethnodiagnostic skill of livestock diseases: a lead to traditional bioprospecting. J Ethnopharmacol 84:79–83CrossRefGoogle Scholar
  52. Orsomando G, Agostinelli S, Bramucci M, Cappellacci L, Damiano S, Lupidi G, Maggi F, Ngahang Kamte SL, Biapa Nya PC, Papa F, Petrelli D, Quassinti L, Sorci L, Vitali LA, Petrelli R (2016) Mexican sunflower (Tithonia diversifolia, Asteraceae) volatile oil as aselective inhibitor of Staphylococcus aureus nicotinatemononucleotide adenylyltransferase (NadD). Ind Crop Prod 85:181–189CrossRefGoogle Scholar
  53. Osei-Safo D, Addae-Mensah I, Garneau FX, Koumaglo HK (2010) A comparative study of the antimicrobial activity of the leaf EOs of chemo-varieties of Clausena anisata (Willd.) Hook. f. ex Benth. Ind Crop Prod 32:634–638CrossRefGoogle Scholar
  54. Pavela R (2008) Acute and synergistic effects of some monoterpenoid EO compounds on the house fly (Musca domestica L.) J Essent Oil Bearing Plants 11:451–459CrossRefGoogle Scholar
  55. Pavela R (2011) Insecticidal properties of phenols on Culex quinquefasciatus Say and Musca domestica L. Parasitol Res 109:1547–1553CrossRefGoogle Scholar
  56. Pavela R (2014) Acute, synergistic and antagonistic effects of some aromatic compounds on the Spodoptera littoralis Boisd. (Lep., Noctuidae) larvae. Ind Crop Prod 60:247–258CrossRefGoogle Scholar
  57. Pavela R (2015a) EOs for the development of eco-friendly mosquito larvicides: a review. Ind Crop Prod 76:174–187CrossRefGoogle Scholar
  58. Pavela R (2015b) Acute toxicity and synergistic and antagonistic effects of the aromatic compounds of some EOs against Culex quinquefasciatus Say larvae. Parasitol Res 114:3835–3853CrossRefGoogle Scholar
  59. Pavela R (2016) History, presence and perspective of using plant extracts as commercial botanical insecticides and farm products for protection against insects—a review. Plant Protect Sci 52:229–241CrossRefGoogle Scholar
  60. Pavela R, Benelli G (2016a) Ethnobotanical knowledge on botanical repellents employed in the African region against mosquito vectors—a review. Exp Parasitol 167:103–108CrossRefGoogle Scholar
  61. Pavela R, Benelli G (2016b) EOs as eco-friendly biopesticides? Challenges and constraints. Trends Plant Sci 21:1000–1007CrossRefGoogle Scholar
  62. Pavela R, Govindarajan M (2017) The EO from Zanthoxylum monophyllum a potential mosquito larvicide with low toxicity to the non-target fish Gambusia affinis. J Pest Sci 90:369–378CrossRefGoogle Scholar
  63. Pavela R, Vrchotova N, Triska J (2009) Mosquitocidal activities of thyme oils (Thymus vulgaris L.) against Culex quinquefasciatus (Diptera: Culicidae). Parasitol Res 105:1365–1370CrossRefGoogle Scholar
  64. Pavela R, Canale A, Mehlhorn H, Benelli G (2016a) Application of ethnobotanical repellents and acaricides in prevention, control and management of livestock ticks: a review. Res Vet Sci 109:1–9CrossRefGoogle Scholar
  65. Pavela R, Maggi F, Mbuntcha H, Woguem V, Fogang HPD, Womeni HM, Tapondjou LA, Barboni L, Nicoletti M, Canale A, Benelli G (2016b) Traditional herbal remedies and dietary spices from Cameroon as novel sources of larvicides against filariasis mosquitoes? Parasitol Res 115:4617–4626CrossRefGoogle Scholar
  66. Pavela R, Stepanycheva E, Shchenikova A, Chermenskaya T, Petrova M (2016c) EOs as prospective fumigants against Tetranychus urticae Koch. Ind Crop Prod 94:755–761CrossRefGoogle Scholar
  67. Pereira DM, Ferreres F, Oliveira J, Valentão P, Andrade PB, Sottomayor M (2009) Targeted metabolite analysis of Catharanthus roseus and its biological potential. Food Chem Toxicol 47:1349–1354CrossRefGoogle Scholar
  68. Pino JA, Marbot R, Real IM (2003) EO of Chenopodium ambrosioides L. from Cuba. J Essent Oil Res 15:213–214CrossRefGoogle Scholar
  69. Pollack Y, Segal R, Golenser J (1990) The effect of ascaridole on the in vitro development of Plasmodium falciparum. Parasitol Res 76:570–572CrossRefGoogle Scholar
  70. Posner GH, O’Neill PM (2004) Knowledge of the proposed chemical mechanism of action and cytochrome P450 metabolism of antimalarial trioxanes like artemisinin allows rational design of new antimalarial peroxides. Acc Chem Res 37:397–404CrossRefGoogle Scholar
  71. Potawale SE, Luniya KP, Mantri RA, Mehta UK, Waseem MD, Sadiq MD, Vetal YD, Deshmukh RS (2008) Chenopodium ambrosioides: an ethnopharmacological review. Pharmacol Online 2:272–286Google Scholar
  72. Ramar M, Paulraj GM, Ignacimuthu S (2013) Preliminiary screening of plant essential oils against larvae of Culex quinquefasciatus Say (Diptera: Culicidae). Afric J Biotechnol 12:6480–6483CrossRefGoogle Scholar
  73. Rattan RS (2010) Mechanism of action of insecticidal secondary metabolites of plant origin. Crop Prot 29:913–920CrossRefGoogle Scholar
  74. Reisch J, Adesina SK, Berbenthal D, Hussain RA (1985) Chemosystematics in the Rutaceae: volatile constituents of Clausena anisata (Willd.) Oliv. Pericarp, root and leaf. Sci Pharm 53:153–158Google Scholar
  75. Rizzati V, Briand O, Guillou H, Gamet-Payrastre L (2016) Effects of pesticide mixtures in human and animal models: an update of the recent literature. Chem Biol Interact 254:231–246CrossRefGoogle Scholar
  76. Sagrero-Nieves L, Bartley JP (1995) Volatile constituents from the leaves of Chenopodium ambrosioides L. J Essent Oil Res 7:221–223CrossRefGoogle Scholar
  77. Santiago JA, Cardoso MG, Batista LR, de Castro EM, Teixeira ML, Pires MF (2016) EO from Chenopodium ambrosioides L.: secretory structures, antibacterial and antioxidant activities. Acta Scientiarum 38:139–147Google Scholar
  78. Senatore F, Oliviero F, Scandolera E, Taglialatela-Scafati O, Roscigno G, Zaccardelli M, De Falco E (2013) Chemical composition, antimicrobial and antioxidant activities of anethole-rich oil from leaves of selected varieties of fennel [Foeniculum vulgare Mill. ssp. vulgare var. azoricum (Mill.) Thell]. Fitoterapia 90:214–219CrossRefGoogle Scholar
  79. Senthilkumar A, Venkatesalu V (2009) Phytochemical analysis and antibacterial activity of the EO of Clausena anisata (Willd.) Hook. f. ex Benth. Int J Integr Biol 5:116–120Google Scholar
  80. Shah RM, Abbas N, Shad SA, Sial AA (2015) Selection, resistance risk assessment, and reversion toward susceptibility of pyriproxyfen in Musca domestica L. Parasitol Res 114:487–494CrossRefGoogle Scholar
  81. Singh HP, Batish DR, Kohli RK, Mittal S, Yadav S (2008) Chemical composition of EO from leaves of Chenopodium ambrosioides from Chandigarh, India. Chem Nat Compd 44:378–379CrossRefGoogle Scholar
  82. Tahir HM, Hussain K, Khan AA, Naseem S, Malik HT, Butt A, Yaqoob R (2013) Susceptibility of Culex quinquefasciatus (Diptera: Culicidae) to malathion in Sargodha district, Pakistan. Open J Anim Sci 3:1–4CrossRefGoogle Scholar
  83. Tak J-H, Jovel E, Isman MB (2016) Contact, fumigant and cytotoxic activities of thyme and lemongrass oils against larvae and an ovarian cell line of the cabbage looper, Trichoplusia ni. J Pest Sci 89:183–193CrossRefGoogle Scholar
  84. Tapondjou AL, Adler C, Bouda H, Reichmuth CH (2002a) Ability of products derived from the leaves of Clausena anisata to protect stored grains from attack by Callosobruchus maculatus and C. chinensis (Coleoptera, Bruchidae). IOBC Bulletin 25:153–160Google Scholar
  85. Tapondjou LA, Adler C, Bouda H, Fontem DA (2002b) Efficacy of powder and EO from Chenopodium ambrosioides leaves as postharvest grain protectants against six-stored product beetles. J Stored Prod Res 38:395–402CrossRefGoogle Scholar
  86. Uwaifo AO (1984) The mutagenicities of seven coumarin derivatives and a furan derivative (nimbolide) isolated from three medicinal plants. J Toxicol Environ Health 13:521–530CrossRefGoogle Scholar
  87. Vadivalagan C, Pushparaj K, Murugan K, Panneerselvam C, Del Serrone P, Benelli G (2017) Exploring genetic variation in haplotypes of the filariasis vector Culex quinquefasciatus (Diptera: Culicidae) through DNA barcoding. Acta Tropica 169:43–50.  https://doi.org/10.1016/j.actatropica.2017.01.020 CrossRefGoogle Scholar
  88. Ward M, Benelli G (2017) Avian and simian malaria: do they have a cancer connection? Parasitol Res 116:839–845CrossRefGoogle Scholar
  89. Wei H, Liu J, Li B, Zhan Z, Chen Y, Tian H, Lin S, Gu X (2015) The toxicity and physiological effect of EO from Chenopodium ambrosioides against the diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae). Crop Prot 76:68–74CrossRefGoogle Scholar
  90. WHO (1991) The housefly. Training and information guide (intermediate level). Geneva, (unpublished document WHO/VBC/90.987; available on request from Division of Control of Tropical Diseases, World Health Organization, 1211 Geneva 27, Switzerland)Google Scholar
  91. WHO (1996) Report of the WHO informal consultation on the evaluation and testing of insecticides. CTD/WHOPES/IC/96.1Google Scholar
  92. Yaouba A, Tatsadjieu LN, Dongmo PMJ, Etoa FX, Mbofung CMF, Amvam Zollo PH, Menut C (2011) Evaluation of Clausena anisata EO from Cameroon for controlling food spoilage fungi and its potential use as an antiradical agent. Nat Prod Commun 6:1367–1371Google Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Roman Pavela
    • 1
  • Filippo Maggi
    • 2
  • Giulio Lupidi
    • 2
  • Hélène Mbuntcha
    • 3
    • 4
  • Verlaine Woguem
    • 3
    • 4
  • Hilaire Macaire Womeni
    • 4
  • Luciano Barboni
    • 5
  • Léon Azefack Tapondjou
    • 3
  • Giovanni Benelli
    • 6
  1. 1.Crop Research InstitutePrague 6Czech Republic
  2. 2.School of PharmacyUniversity of CamerinoCamerinoItaly
  3. 3.Laboratory of Environmental and Applied Chemistry, Faculty of ScienceUniversity of DschangDschangCameroon
  4. 4.Laboratory of Biochemistry of Medicinal Plants, Food Science and Nutrition, Faculty of ScienceUniversity of DschangDschangCameroon
  5. 5.School of Science and TechnologyUniversity of CamerinoCamerinoItaly
  6. 6.Department of Agriculture, Food and EnvironmentUniversity of PisaPisaItaly

Personalised recommendations