Environmental Science and Pollution Research

, Volume 25, Issue 11, pp 10515–10525 | Cite as

The crop-residue of fiber hemp cv. Futura 75: from a waste product to a source of botanical insecticides

  • Giovanni BenelliEmail author
  • Roman Pavela
  • Giulio Lupidi
  • Massimo Nabissi
  • Riccardo Petrelli
  • Stephane L. Ngahang Kamte
  • Loredana Cappellacci
  • Dennis Fiorini
  • Stefania Sut
  • Stefano Dall’Acqua
  • Filippo Maggi
Plant-borne compounds and nanoparticles: challenges for medicine, parasitology and entomology


In the attempt to exploit the potential of the monoecious fiber hemp cv. Futura 75 in new fields besides textile, cosmetics and food industry, its crop-residue given by leaves and inflorescences was subjected to hydrodistillation to obtain the essential oils. These are niche products representing an ideal candidate for the development of natural insecticides for the control and management of mosquito vectors, houseflies and moth pests. After GC-MS analysis highlighting a safe and legal chemical profile (THC in the range 0.004–0.012% dw), the leaf and inflorescence essential oils were investigated for the insecticidal potential against three insect targets: the larvae of Culex quinquefasciatus and Spodoptera littoralis and the adults of Musca domestica. The essential oil from inflorescences, showing (E)-caryophyllene (21.4%), myrcene (11.3%), cannabidiol (CBD, 11.1%), α-pinene (7.8%), terpinolene (7.6%), and α-humulene (7.1%) as the main components, was more effective than leaf oil against these insects, with LD50 values of 65.8 μg/larva on S. littoralis, 122.1 μg/adult on M. domestica, and LC50 of 124.5 μl/l on C. quinquefasciatus larvae. The hemp essential oil moderately inhibited the acetylcholinesterase (AChE), which is a target enzyme in pesticide science. Overall, these results shed light on the future application of fiber hemp crop-residue for the development of effective, eco-friendly and sustainable insecticides.


Cannabis sativa Crop residue Essential oil Culex quinquefasciatus Musca domestica Spodoptera littoralis 



Philippe Garrigues and three anonymous reviewers kindly improved an earlier version of our manuscript. The authors are grateful to Michele Grossi, Luigi Corradini, and La Biologica Soc. Coop. Agr. for kindly providing the crop-residue of hemp cv. Futura 75 for studies. 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 University of Camerino (Fondo di Ateneo per la Ricerca, FAR 2014/2015, FPI 000044) for financial support.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.


  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. Carol Stream, AlluredGoogle Scholar
  3. Amaducci MT (1969) Ricerche sulla tecnica colturale delle canape monoiche utilizzate per la fabbricazione di carte pregiate. Sementi Elette 3:166–177Google Scholar
  4. Baldwin JL, Graves JB (1991) Cotton insect pest management. LA Coop Ext Serv Bull 1829Google Scholar
  5. Bedini S, Flamini G, Cosci F, Ascrizzi R, Benelli G, Conti B (2016) Cannabis sativa and Humulus lupulus essential oils as novel control tools against the invasive mosquito Aedes albopictus and fresh watersnail Physella acuta. Ind Crop Prod 85:318–323CrossRefGoogle Scholar
  6. Benelli G (2015a) Research in mosquito control: current challenges for a brighter future. Parasitol Res 114:2801–2805CrossRefGoogle Scholar
  7. 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
  8. Benelli G (2016a) Plant-mediated biosynthesis of nanoparticles as an emerging tool against mosquitoes of medical and veterinary importance: a review. Parasitol Res 115:23–34CrossRefGoogle Scholar
  9. Benelli G (2016b) Green synthesized nanoparticles in the fight against mosquito-borne diseases and cancer – a brief review. Enzym Microb Technol 95:58–68CrossRefGoogle Scholar
  10. Benelli G (2017a) Plant-borne compounds and nanoparticles: challenges for medicine, parasitology and entomology – GREEN-NANO-PEST&DRUGS. Environ Sci Poll Res.
  11. Benelli G (2017b) Commentary: data analysis in bionanoscience – issues to watch for. J Clust Sci 28:11–14CrossRefGoogle Scholar
  12. Benelli G (2018) Gold nanoparticles – against parasites and insect vectors. Acta Tropica.
  13. Benelli G, Beier J (2017) Current vector control challenges in the fight against malaria. Acta Trop 174:91–96CrossRefGoogle Scholar
  14. Benelli G, Mehlhorn H (2016) Declining malaria, rising dengue and Zika virus: insights for mosquito vector control. Parasitol Res 115:1747–1754CrossRefGoogle Scholar
  15. Benelli G, Romano D (2017) Mosquito vectors of Zika virus. Entomol Gen,
  16. 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
  17. 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 96:186–195Google Scholar
  18. Benelli G, Pavela R, Canale A, Cianfaglione K, Ciaschetti G, Conti F, Nicoletti M, Senthil-Nathan S, Mehlhorn H, Maggi F (2017b) Acute larvicidal toxicity of five essential oils (Pinus nigra, Hyssopus officinalis, Satureja montana, Aloysia citrodora and Pelargonium graveolens) against the filariasis vector Culex quinquefasciatus: synergistic and antagonistic effects. Parasitol Int 66:166–171Google Scholar
  19. Bertoli A, Tozzi S, Pistelli L, Angelini LG (2010) Fiber hemp inflorescences: from crop-residues to essential oil production. Ind Crop Prod 32:329–337CrossRefGoogle Scholar
  20. Borges RS, Batista Jr J, Viana RB, Baetas AC, Orestes E, Andrade MA, Káthia M, Honório KM, Albérico BF, da Silva ABF (2013) Understanding the molecular aspects of tetrahydrocannabinol and cannabidiol as antioxidants. Molecules 18:12663–12674Google Scholar
  21. Callaway JC (2004) Hempseed as a nutritional resource, an overview. Euphytica 140:65–72CrossRefGoogle Scholar
  22. Calzolari D, Magagnini G, Lucini L, Grassi G, Appendino GB, Amaducci S (2017) High added-value compounds from Cannabis threshing residues. Ind Crop Prod 108:558–563CrossRefGoogle Scholar
  23. 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 47:310–315CrossRefGoogle Scholar
  24. Choi WS, Park BS, Lee YH, Jang DY, Yoon HY, Lee SE (2006) Fumigant toxicities of essential oils and monoterpenes against Lycoriella mali adults. Crop Prot 25:398–401CrossRefGoogle Scholar
  25. Christoph M, Mediavilla V (1998) Factors influencing the yield and the quality of hemp (Cannabis sativa L.) essential oil. J Int Hemp Association 5:16–20Google Scholar
  26. Del Gatto A, Laureti D, Crescentini P (2001) Un biennio di valutazione di varietà di canapa. Inf Agrar 16:39–42Google Scholar
  27. ElSohly M, Gul W (2014) Constituents of Cannabis Sativa. In: Pertwee RG (ed) Handbook of cannabis. Oxford University Press, Oxford, pp 3–22CrossRefGoogle Scholar
  28. EPPO (1990) Specific quarantine requirements. EPPO Technical Documents, No. 1008. European and Mediterranean Plant Protection Organization, Paris, FranceGoogle Scholar
  29. Finney DJ (1971) Probit analysis. Cambridge University Press, LondonGoogle Scholar
  30. FFNSC 2 (2012) Flavors and Fragrances of Natural and Synthetic Compounds. Mass spectral database. Kyoto, Shimadzu CorpsGoogle Scholar
  31. Fournier G, Paris MR, Fourniat MC, Quero AM (1978) Activité bactériostatique d’huiles essentielles de Cannabis sativa L. [Bacteriostatic activity of Cannabis sativa L. essential oil.] Ann Pharm Fr 36:603–606Google Scholar
  32. Hall W, Solowij N (1998) Adverse effects of cannabis. Lancet 352:1611–1616CrossRefGoogle Scholar
  33. Hampson AJ, Grimaldi M, Axelrod J, Wink D (1998) Cannabidiol and (2)D9-tetrahydrocannabinol are neuroprotective antioxidants. Proc Natl Acad Sci U S A 95:8268–8273CrossRefGoogle Scholar
  34. Happyana N, Kayser O (2016) Monitoring metabolite profiles of Cannabis sativa L. trichomes during flowering period using 1H NMR-based metabolomics and real-time PCR. Planta Med 82:1217–1223CrossRefGoogle Scholar
  35. Hemphill JK, Turner JC, Mahlberg PG (1980) Cannabinoid content of individual plant organs from different geographical strains of Cannabis sativa L. J Nat Prod 43:112–122CrossRefGoogle Scholar
  36. Hendriks H, Malingre TM, Batterman S, Bos R (1975) Mono- and sesquiterpene hydrocarbons of the essential oil of Cannabis sativa. Phytochemistry 14:814–815CrossRefGoogle Scholar
  37. Isman B (2006) Botanical insecticides, deterrents, and repellents in modern agriculture and an increasingly regulated world. Annu Rev Entomol 51:45–66CrossRefGoogle Scholar
  38. Jalees S, Sharma SK, Rahman SJ, Verghese T (1993) Evaluation of insecticidal properties of an indigenous plant, Cannabis sativa Linn., against mosquito larvae under laboratory conditions. J Entomol Res 17:117–120Google Scholar
  39. Jyotshna SN, Singh B, Chanda D, Shanker K (2015) Chemical composition and acetylcholinesterase inhibitory activity of Artemisia maderaspatana essential oil. Pharm Biol 53:1677–1683CrossRefGoogle Scholar
  40. Malingre T, Hendriks H, Batterman S, Bos R (1973) The presence of cannabinoid components in the essential oil of Cannabis sativa L. Pharrn Weekbl 108:549–552Google Scholar
  41. Malingré T, Hendriks H, Batterman S, Bos R, Visser J (1975) The essential oil of Cannabis sativa. Planta Med 28:56–61CrossRefGoogle Scholar
  42. McPartland JM (1997) Cannabis as repellent and pesticide. J Int Hemp Association 4:89–94Google Scholar
  43. Mediavilla V, Steinemann S (1997) Essential oil of Cannabis sativa L. strains. J Int Hemp Association 4:80–82Google Scholar
  44. Miyazawa M, Nakahashi H, Usami A, Matsuda N (2016) Chemical composition, aroma evaluation, and inhibitory activity towards acetylcholinesterase of essential oils from Gynura bicolor DC. J Nat Med 70:282–289CrossRefGoogle Scholar
  45. Morshedloo MR, Quassinti L, Bramucci M, Lupidi G, Maggi F (2017) Chemical composition, antioxidant activity and cytotoxicity on tumor cells of the essential oil from flowers of Magnolia grandiflora cultivated in Iran. Nat Prod Res
  46. Mukhtar T, Kayani MZ, Hussain MA (2013) Nematicidal activities of Cannabis sativa L. and Zanthoxylum alatum Roxb. Against Meloidogyne incognita. Ind Crop Prod 42:447–453CrossRefGoogle Scholar
  47. 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
  48. Nissen L, Zatta A, Stefanini I, Grandi S, Sgorbati B, Biavati B, Monti A (2010) Characterization and antimicrobial activity of essential oils of industrial hemp varieties (Cannabis sativa L.) Fitoterapia 81:413–419CrossRefGoogle Scholar
  49. NIST 08 (2008) National Institute of Standards and Technology mass spectral library (NIST/EPA/NIH). Gaithersburg, National Institute of Standards and TechnologyGoogle Scholar
  50. Novak J, Franz C (2003) Composition of the essential oils and extracts of two populations of Cannabis sativa L. ssp. spontanea from Austria. J Essent Oil Res 15:158–160Google Scholar
  51. Novak J, Zitterl-Eglseer K, Deansand SG, Franz C (2001) Essential oils of different cultivars of Cannabis sativa L. and their antimicrobial activity. Flavour Fragr J 16:259–262CrossRefGoogle Scholar
  52. OEPP/EPPO (2015) EPPO Standards PM 7/124(1) Diagnostic protocol for Spodoptera littoralis, Spodoptera litura, Spodoptera frugiperda, Spodoptera eridania. Bull OEPP/EPPO Bull 34:257–270Google Scholar
  53. Pate DW (1994) Chemical ecology of Cannabis. J Int Hemp Association 1:32–37Google Scholar
  54. Pavela R (2008) Acute and synergistic effects of some monoterpenoid essential oil compounds on the house fly (Musca domestica L.) J Essen Oil Bear Pl 11:451–459CrossRefGoogle Scholar
  55. Pavela R (2015) Essential oils for the development of eco-friendly mosquito larvicides: a review. Ind Crop Prod 76:174–187CrossRefGoogle Scholar
  56. 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 Prot Sci 52:229–241CrossRefGoogle Scholar
  57. Pavela R, Benelli G (2016a) Ethnobotanical knowledge on botanical repellents employed in the African region against mosquito vectors - a review. Exp Parasitol 167:103–108Google Scholar
  58. Pavela R, Benelli G (2016b) EOs as eco-friendly biopesticides? Challenges and constraints. Trends Plant Sci 21:1000–1007Google Scholar
  59. Pavela R, Žabka M, Bednář J, Tříska J, Vrchotová N (2016) New knowledge for yield, composition and insecticidal activity ofessential oils obtained from the aerial parts or seeds of fennel (Foeniculum vulgare Mill.) Ind Crop Prod 83:275–282Google Scholar
  60. 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
  61. Perry NS, Houghton PJ, Theobald A, Jenner P, Perry EK (2000) In-vitro inhibition of human erythrocyte acetylcholinesterase by Salvia lavandulaefolia essential oil and constituent terpenes. J Pharm Pharmacol 52:895–902CrossRefGoogle Scholar
  62. Pertwee RG (2006) Cannabinoid pharmacology: the first 66 years. Br J Pharmacol 147:S163–S171CrossRefGoogle Scholar
  63. Potter DJ (2009) The Propagation, Characterisation and Optimisation of Cannabis sativa L. as a Phytopharmaceutical. Pharmaceutical Sciences, King’s College, LondonGoogle Scholar
  64. Ranalli P, Venturi G (2004) Hemp as a raw material for industrial applications. Euphytica 140:1–6CrossRefGoogle Scholar
  65. Regulation (EC) No 206/ (2004) of the European Parliament and of the Council amending Regulation (EC) No 2316/1999 laying down detailed rules for the application of Council Regulation (EC) No 1251/1999 establishing a support system for producers of certain arable crops. Offic J Eur Commun L34: 33Google Scholar
  66. Rehman MSU, Rashid N, Saif A, Mahmood T, Han J-I (2013) Potential of bioenergy production from industrial hemp (Cannabis sativa): Pakistan perspective. Renew Sust Energ Rev 18:154–164CrossRefGoogle Scholar
  67. Ross SA, ElSohly MA (1996) The volatile oil composition of fresh and air-dried buds of Cannabis sativa. J Nat Prod 59:49–51CrossRefGoogle Scholar
  68. 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
  69. Struik PC, Amaducci S, Bullard MJ, Stutterheim NC, Venturi G, Cromack HTH (2000) Agronomy of fiber hemp (Cannabis sativa L.) in Europe. Ind Crop Prod 11:107–118CrossRefGoogle Scholar
  70. Thalhamer B, Himmelsbach M, Buchberger W (2017) Trace level determination of Δ9-tetrahydrocannabinol in a perfume using liquid chromatography high resolution tandem mass spectrometry and gas chromatography mass spectrometry. Flavour Fragr J 32:46–53CrossRefGoogle Scholar
  71. Thomas TG, Sharma SK, Prakash A, Sharma BR (2000) Insecticidal properties of essential oil of Cannabis sativa Linn. Against mosquito larvae. Entomon 25:21–24Google Scholar
  72. Tiwary M, Naik SN, Tewary DK, Mittal PK, Yadav S (2007) Chemical composition and larvicidal activities of the essential oil of Zanthoxylum armatum DC (Rutaceae) against three mosquito vectors. J Vector Borne Dis 44:198–204Google Scholar
  73. 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 Trop 169:43–50CrossRefGoogle Scholar
  74. Vera SS, Zambrano DF, Méndez-Sanchez SC, Rodríguez-Sanabria F, Stashenko EE, Luna JED (2014) Essential oils with insecticidal activity against larvae of Aedes aegypti (Diptera: Culicidae). Parasitol Res 113:2647–2654CrossRefGoogle Scholar
  75. Verma RS, Padalia RC, Verma SK, Chauhan A, Darokar MP (2014) The essential oil of ‘bhang’ (Cannabis sativa L.) for non-narcotic applications. Curr Sci 107:645–650Google Scholar
  76. Wanas AS, Radwan MM, Mehmedic Z, Jacob M, Khan IA, Elsohly MA (2016) Antifungal activity of the volatiles of high potency Cannabis sativa L. against Cryptococcus neoformans. Rec Nat Prod 10:214–220Google Scholar
  77. 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, 1211Geneva 27, Switzerland)Google Scholar
  78. WHO (1996) Report of the WHO informal consultation on the evaluation and testing of insecticides. CTD/WHOPES/IC/96.1. Geneva.
  79. WHO (2012) Handbook for integrated vector management. World Health Organization, GenevaGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Giovanni Benelli
    • 1
    • 2
    Email author
  • Roman Pavela
    • 3
  • Giulio Lupidi
    • 4
  • Massimo Nabissi
    • 4
  • Riccardo Petrelli
    • 4
  • Stephane L. Ngahang Kamte
    • 4
  • Loredana Cappellacci
    • 4
  • Dennis Fiorini
    • 5
  • Stefania Sut
    • 6
  • Stefano Dall’Acqua
    • 6
  • Filippo Maggi
    • 4
  1. 1.Department of Agriculture, Food and EnvironmentUniversity of PisaPisaItaly
  2. 2.The BioRobotics InstituteScuola Superiore Sant’AnnaPontederaItaly
  3. 3.Crop Research InstitutePrague 6Czech Republic
  4. 4.School of PharmacyUniversity of CamerinoCamerinoItaly
  5. 5.School of Sciences and TechnologyUniversity of CamerinoCamerinoItaly
  6. 6.Department of Pharmaceutical and Pharmacological Sciences, Natural Product LaboratoryUniversity of PadovaPadovaItaly

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