Skip to main content

Advertisement

Log in

Facile synthesis of silver nanoparticles using harmala alkaloids and their insecticidal and growth inhibitory activities against the khapra beetle

  • Original Paper
  • Published:
Journal of Pest Science Aims and scope Submit manuscript

Abstract

In order to find new, less toxic and eco-friendly pest control agents, natural products are considered to be alternative options of potentially active compounds. In this context, the aim of the present study was the isolation and structural elucidation of the β-carboline and quinazoline alkaloids of Peganum harmala L. seeds. Silver nanoparticles (AgNPs) were prepared using alkaloids through a green synthesis procedure. Harmala alkaloids and their AgNPs showed considerable insecticidal and growth inhibitory activities against khapra beetle, Trogoderma granarium (Everts) (Coleoptera: Dermestidae). On a toxicity bioassay using treated filter papers, the total harmala alkaloids (THAs) were the most toxic followed by harmaline, harmine and harmalol, where LC50’s ranged between (30.6–61.7 µg/cm2) and (24.4–46.1 µg/cm2) 24 h post-treatment against larvae and adults, respectively. The two quinazolines, vasicine and vasicinone, showed moderate to weak activities. At 48 h post-exposure, efficacy of all alkaloids was increased. When tested as AgNPs (size 22.5–66.2 nm diameter), toxicity of alkaloids, especially the β-carbolines, was strongly increased, where LC50 values ranged between (4.7–11.4 µg/cm2) and (4.1–10.2 µg/cm2) 48 h post-treatment against larvae and adults, respectively. Feeding the 2nd instar larvae AgNPs-treated grains at sublethal concentrations led to significant drawbacks on the normal growth and development of the insect. These effects appeared as a high percentage of malformed larvae and pupae, a prolonged life span and a significant reduction in adult emergence. Results suggest the potential of using harmala alkaloids and their AgNPs as a natural approach for controlling T. granarium.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Abbott WS (1925) A method for computing the effectiveness of an insecticide. J Econ Entomol 18:265–267

    Article  CAS  Google Scholar 

  • Abdel-Sattar E, Zaitoun A, Farag M, El Gayed S, Harraz F (2010) Chemical composition, insecticidal and insect repellent activity of Schinus molle L. leaf and fruit essential oils against Trogoderma granarium and Tribolium castaneum. Nat Prod Res 24(3):226–235

    Article  CAS  PubMed  Google Scholar 

  • Arbain R, Othman M, Palaniandy S (2011) Preparation of iron oxide nanoparticles by mechanical milling. Miner Eng 24:1–9

    Article  CAS  Google Scholar 

  • Atiyeh BS, Costagliola M, Hayek SN, Dibo SA (2007) Effect of silver on burn wound infection control and healing: review of the literature. Burns 33:139–148

    Article  PubMed  Google Scholar 

  • Begum NA, Mondal S, Basu S, Laskar RA, Mandal D (2009) Biogenic synthesis of Au and Ag nanoparticles using aqueous solutions of black tea leaf extracts. Colloid Surf B 71(1):113–118

    Article  CAS  Google Scholar 

  • Bell C, Wilson S (1995) Phosphine tolerance and resistance in Trogoderma granarium Everts (Coleoptera: Oermestidae). J Stored Prod Res 31:199–205

    Article  CAS  Google Scholar 

  • Berenbaum M (1989) What is synergy? Pharmacol Rev 41:93–141

    CAS  PubMed  Google Scholar 

  • Berrougui H, Cordero M, Khalil A, Hamamouchi M, Ettiab A, Martín-Marhuenda E, Herrara M (2006) Vasorelaxant effects of harmine and harmaline extracted from Peganum harmala L. seeds in isolated rat aorta. Pharmacol Res 54:150–157

    Article  CAS  PubMed  Google Scholar 

  • Bhattacharyya A, Bhaumik A, Rani PU, Mandal S, Epidi T (2010) Nano-particles—a recent approach to insect pest control. Afr J Biotechnol 9(24):3489–3493

    CAS  Google Scholar 

  • Bollerlbachcer W (1988) The interendocrine regulation of larva-pupal development in the tobacco hornworm, Manduca sexta. J Insect Physiol 34:947–948

    Google Scholar 

  • Bordes P, Pollet E, Avérous L (2009) Nano-biocomposites: biodegradable polyester/nanoclay systems. Prog Polym Sci 34(2):125–155

    Article  CAS  Google Scholar 

  • Borzoui E, Naseri B, Namin FR (2015) Different diets affecting biology and digestive physiology of the khapra beetle, Trogoderma granarium Everts (Coleoptera: Dermestidae). J Stored Prod Res 62:1–7

    Article  Google Scholar 

  • Boukouvala MC, Kavallieratos NG, Athanassiou CG et al (2017) Laboratory evaluation of five novel pyrrole derivatives as grain protectants against Tribolium confusum and Ephestia kuehniella larvae. J Pest Sci 90(2):569–585

    Article  Google Scholar 

  • Bukhari N, Choi J, Jeon C, Park H, Kim W, Khan M, Lee S (2008) Phytochemical studies of the alkaloids from Peganum harmala. Appl Chem 12(1):101–104

    Google Scholar 

  • Chaudhry Q, Scotter M, Blackburn J, Ross B, Boxall A, Castle L, Aitken R, Watkins R (2008) Applications and implications of nanotechnologies for the food sector. Food Addit Contam 25(3):241–258

    Article  CAS  Google Scholar 

  • Dayan FE, Cantrell CL, Duke SO (2009) Natural products in crop protection. Bioorg Med Chem 17(12):4022–4034

    Article  CAS  PubMed  Google Scholar 

  • De A, Bose R, Kumar A, Mozumdar S (2014) Management of insect pests using nanotechnology: as modern approaches. In: De A, Bose R, Kumar A, Mozumdar S (eds) Targeted delivery of pesticides using biodegradable polymeric nanoparticles. Part of the series Springer Briefs in Molecular Science. Springer, New Delhi, pp 29–33

    Chapter  Google Scholar 

  • Deletre E, Chandre F, Barkman B, Menut C, Martina T (2016) Naturally occurring bioactive compounds from four repellent essential oils against Bemisia tabaci whiteflies. Pest Manag Sci 72:179–189

    Article  CAS  PubMed  Google Scholar 

  • Eliopoulos PA (2013) New approaches for tackling the khapra beetle. CAB Int Rev 8(012):1–13

    Google Scholar 

  • Farouk L, Laroubi A, Aboufatima R, Benharref A, Chait A (2008) Evaluation of the analgesic effect of alkaloid extract of Peganum harmala L.: possible mechanisms involved. J Ethnopharmacol 115:449–454

    Article  CAS  PubMed  Google Scholar 

  • Finney DJ (1971) Probit analysis, 3rd edn. Cambridge University Press, London

    Google Scholar 

  • Ge Y, Liu P, Yang R, Zhang L, Chen H, Camara I, Liu Y, Shi W (2015) Insecticidal constituents and activity of alkaloids from Cynanchum mongolicum. Molecules 20:17483–17492

    Article  CAS  PubMed  Google Scholar 

  • Georghiou GP (1990) Overview of insecticide resistance. In: Green MB, LeBaron HM, Moberg WK (eds) Managing resistance to agrochemicals: from fundamental research to practical strategies. American Chemical Society, Washington DC, p 18

  • Hartmann T (1991) Alkaloids. In herbivores; their interaction with secondary plant metabolites. In: Rosenthal GA, Berenbaum MR (eds) The chemical participants, vol 1, 2nd edn. Academic press, San Diego, pp 33–85

    Google Scholar 

  • Henglein A, Linnert T, Mulvaney P (1990) Reduction of Ag+ in aqueous polyanion solution some properties and reactions of long-lived oligomeric silver clusters and metallic silver particles. Berich Bunsen Gesell 94(12):1449–1457

    Article  CAS  Google Scholar 

  • Herraiz T, Guillén H, Arán VJ (2008) Oxidative metabolism of the bioactive and naturally occurring β-carboline alkaloids, norharmane and harmane, by human cytochrome P450 enzymes. Chem Res Toxicol 21(11):2172–2180

    Article  CAS  PubMed  Google Scholar 

  • Herraiz T, González D, Ancín-Azpilicueta C, Arán VJ, Guillén H (2010) β-Carboline alkaloids in Peganum harmala and inhibition of human monoamine oxidase (MAO). Food Chem Toxicol 48:839–845

    Article  CAS  PubMed  Google Scholar 

  • Huang J, Li Q, Sun D, Lu Y, Su Y, Yang X, Wang H, Wang Y, Shao W, He N, Hong J, Chen C (2007) Biosynthesis of silver and gold nanoparticles by novel sundried Cinnamomum camphora leaf. Nanotechnology 18(10):105104–105115

    Article  Google Scholar 

  • Jindal V, Dhaliwal G, Koul O (2013) Pest management in 21st century: roadmap for future. Biopestic Int 9(1):1–22

    Google Scholar 

  • Kanda D, Kaur S, Koul O (2017) A comparative study of monoterpenoids and phenylpropanoids from essential oils against stored grain insects: acute toxins or feeding deterrents. J Pest Sci 90(2):531–545

    Article  Google Scholar 

  • Kartal M, Altun ML, Kurucu S (2003) HPLC method for the analysis of harmol, harmalol, harmine and harmaline in the seeds of Peganum harmala L. J Pharmaceut Biomed 31:263–269

    Article  CAS  Google Scholar 

  • Khot L, Sankaran S, Maja J, Ehsani R, Schuster E (2012) Applications of nanomaterials in agricultural production and crop protection: a review. Crop Prot 35:64–70

    Article  CAS  Google Scholar 

  • Kulkarni NV, Gupta S, Kataria R, Sathyanarayana N (2015) Morphometric analysis and reproductive system studies of Trogoderma granarium Everts (Coleoptera: Dermestidae). Int J Sci Res Publ 5(8):1–8

    Google Scholar 

  • Kumar M, Srivastava C, Garg A (2010) In vitro selection of deltamethrin resistant strain of Trogoderma granarium and its susceptibility to insecticides. Ann Plant Prot Sci 18(1):26–30

    Google Scholar 

  • Lamchouri F, Settaf A, Cherra Y, Hassar M, Zemzami M, Atif N, Nadori EB, Zaid A, Lyoussi B (2000) In vitro cell-toxicity of Peganum harmala alkaloids on cancerous cell-lines. Fitoterapia 71(1):50–54

    Article  CAS  PubMed  Google Scholar 

  • Liu ZL, Ho SH (1999) Bioactivity of the essential oil extracted from Evodia rutaecarpa Hook f. et Thomas against the grain storage insects, Sitophilus zeamais Motsch. and Tribolium castaneum (Herbst). J Stored Prod Res 35(4):317–328

    Article  Google Scholar 

  • Lowe S, Browne M, Boudjelas S, de Poorter M (2000) 100 of the world’s worst invasive alien species: the global invasive species database. http://www.issg.org/booklet.pdf. Invasive Species Specialist Group. The World Conservation Union (IUCN). http://www.issg.org/booklet.pdf

  • Mahmoudian M, Jalilpour H, Salehian P (2002) Toxicity of Peganum harmala: review and a case report. Iran J Pharmacol Ther 1:1–4

    Google Scholar 

  • Margulis-Goshen K, Magdassi S (2013) Nanotechnology: an advanced approach to the development of potent insecticides. In: Ishaaya I, Palli S, Horowitz A (eds) Advanced technologies for managing insect pests. Springer, Dordrecht, pp 295–314

    Chapter  Google Scholar 

  • Moorthi PV, Balasubramanian C, Mohan S (2015) An improved insecticidal activity of silver nanoparticle synthesized by using Sargassum muticum. Appl Biochem Biotechnol 175(1):135–140

    Article  CAS  PubMed  Google Scholar 

  • Navaladian S, Viswanathan B, Viswanath RP, Varadarajan TK (2007) Thermal decomposition as route for silver nanoparticles. Nanoscale Res Lett 2:44–48

    Article  CAS  Google Scholar 

  • Nenaah G (2010) Antibacterial and antifungal activities of (beta)-carboline alkaloids of Peganum harmala (L) seeds and their combination effects. Fitoterapia 81(7):779–782

    Article  CAS  PubMed  Google Scholar 

  • Nenaah G (2011a) Toxic and antifeedant activities of potato glycoalkaloids against Trogoderma granarium (Coleoptera: Dermestidae). J Stored Prod Res 47:185–190

    Article  CAS  Google Scholar 

  • Nenaah G (2011b) Toxicity and growth inhibitory activities of methanol extract and the β-carboline alkaloids of Peganum harmala L. against two coleopteran stored-grain pests.). J Stored Prod Res 47:255–261

    Article  CAS  Google Scholar 

  • Nenaah G (2014a) Chemical composition, insecticidal and repellence activities of essential oils of three Achillea species against the khapra beetle (Coleoptera: Dermestidae). J Pest Sci 87:273–283

    Article  Google Scholar 

  • Nenaah G (2014b) Bioactivity of powders and essential oils of three Asteraceae plants as post-harvest grain protectants against three major coleopteran pests. J Asia Pac Entomol 17:701–709

    Article  CAS  Google Scholar 

  • Nenaah G (2014c) Chemical composition, toxicity and growth inhibitory activities of essential oils of three Achillea species and their nano-emulsions against Tribolium castaneum (Herbst). Ind Crops Prod 53:252–260

    Article  CAS  Google Scholar 

  • Nenaah G, Ibrahim S, Al-Assiuty B (2015) Chemical composition, insecticidal activity and persistence of three Asteraceae essential oils and their nanoemulsions against Callosobruchus maculatus (F.). J Stored Prod Res 61:9–16

    Article  Google Scholar 

  • Oberdörster G, Oberdörster E, Oberdörster J (2005) Nanotoxicology: discipline evolving from studies of ultrafine particles. Environ Health Perspect 113(7):823–839

    Article  PubMed  PubMed Central  Google Scholar 

  • Patil CD, Patil SV, Borase HP, Salunke BK, Salunkhe RB (2012) Larvicidal activity of silver nanoparticles synthesized using Plumeria rubra plant latex against Aedes aegypti and Anopheles stephensi. Parasitol Res 110(5):1815–1822

    Article  PubMed  Google Scholar 

  • Prakash P, Gnanaprakasam P, Emmanuel R, Arokiyaraj S, Saravanan M (2013) Green synthesis of silver nanoparticles from leaf extract of Mimusops elengi Linn. For enhanced antibacterial activity against multi drug resistant clinical isolates. Colloid Surf B 108:255–259

    Article  CAS  Google Scholar 

  • Priyadarshini KA, Murugan K, Panneerselvam C, Ponarulselvam S, Hwang J-S, Nicoletti M (2012) Biolarvicidal and pupicidal potential of silver nanoparticles synthesized using Euphorbia hirta against Anopheles stephensi Liston (Diptera: Culicidae). Parasitol Res 111(3):997–1006

    Article  PubMed  Google Scholar 

  • Rajakumar G, Abdul Rahuman A (2011) Larvicidal activity of synthesized silver nanoparticles using Eclipta prostrata leaf extract against filariasis and malaria vector. Acta Trop 118:196–203

    Article  CAS  PubMed  Google Scholar 

  • Rharrabe K, Bakrim A, Ghailani N, Sayah F (2007) Bioinsecticidal effect of harmaline on Plodia interpunctella development (Lepidoptera: Pyralidae). Pestic Biochem Phys 89:137–145

    Article  CAS  Google Scholar 

  • Scott I, Puniani E, Durst T, Phelps D, Merali S, Assabgui R, Sanchez-Vindas P, Poveda L, Philogene B, Arnason J (2002) Insecticidal activity of Piper tuberculatum Jacq. extracts: synergistic interaction of Piper amides. Agric Forest Entomol 4:137–144

    Article  Google Scholar 

  • Scott I, Tolman J, MacArthur D (2015) Insecticide resistance and cross-resistance development in Colorado potato beetle Leptinotarsa decemlineata Say (Coleoptera: Chrysomelidae) populations in Canada 2008–2011. Pest Manag Sci 71(5):712–721

    Article  CAS  PubMed  Google Scholar 

  • Silver S (2003) Bacterial silver resistance: molecular biology and uses and misuses of silver compounds. FEMS Microbiol Rev 27:341–353

    Article  CAS  PubMed  Google Scholar 

  • Sreeram KS, Nidin M, Nair BU (2008) Microwave assisted template synthesis of silver nanoparticles. Bull Mater Sci 31(7):937–942

    Article  CAS  Google Scholar 

  • Starowicz M, Stypula B, Banas J (2006) Electrochemical synthesis of silver nanoparticles. Electrochem Commun 8(2):227–230

    Article  CAS  Google Scholar 

  • Stepanek P (1993) Data analysis in dynamic light scattering. In: Brown W (ed) Dynamic light scattering: the method and some applications. Clarendon Press, Oxford, pp 177–241

    Google Scholar 

  • Sun H, Fu X, Chen X, Shi WP (2012) Toxicity and influences of the alkaloids from Cynanchum mongolicum AL. Iljinski (Asclepiadaceae) on growth and cuticle components of Spodoptera litura Fabricius (Noctuidae) larvae. Nat Prod Res 26:903–912

    Article  CAS  PubMed  Google Scholar 

  • Tayoub G, Abu A, Ghanem I (2012) Fumigant activity of leaf essential oil from Myrtus communis L. against the khapra Beetle. Int J Med Arom Plants 2(1):207–213

    Google Scholar 

  • Viljoen JH (1990) The occurrence of Trogoderma (Coleoptera: Dermestidae) and related species in southern Africa with special reference to T. granarium and its potential to become established. J Stored Prod Res 26(1):43–51

    Article  Google Scholar 

  • Weiss J, Gaysinksy S, Davidson M, Mcclements J (2009) Nanostructured encapsulation systems: food antimicrobials. In: Barbosa C, Gnovas GV, Mortimer A, Lineback D, Spiess W, Buckle K (eds) IUFOST world congress book: global issues in food science and technology. Elsevier, Amsterdam, p 520

    Google Scholar 

  • Wink M (1988) Plant breeding: importance of plant secondary metabolites for protection against pathogens and herbivores. Theor Appl Genet 75:225–233

    Article  CAS  Google Scholar 

  • Yeo SY, Lee HJ, Jeong SH (2003) Preparation of nanocomposite fibers for permanent antibacterial effect. J Mater Sci 38:2143–2147

    Article  CAS  Google Scholar 

  • Zayed R, Wink M (2005) β-Carboline and quinoline alkaloids in root cultures and intact plants of Peganum harmala. Z Naturforsch 60c:451–458

    Google Scholar 

Download references

Acknowledgements

This study was supported by a research fund from the Deanship of Scientific Research, Najran University, Saudi Arabia (Grant No. NU/ESCI/15/022).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gomah E. Nenaah.

Ethics declarations

Conflict of interest

The authors declare that there is no conflict to disclose.

Additional information

Communicated by C.G. Athanassiou.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Almadiy, A.A., Nenaah, G.E. & Shawer, D.M. Facile synthesis of silver nanoparticles using harmala alkaloids and their insecticidal and growth inhibitory activities against the khapra beetle. J Pest Sci 91, 727–737 (2018). https://doi.org/10.1007/s10340-017-0924-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10340-017-0924-2

Keywords

Navigation