Skip to main content
SpringerLink
Log in

A comparative study of monoterpenoids and phenylpropanoids from essential oils against stored grain insects: acute toxins or feeding deterrents

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

Abstract

The relationship between the acute toxicity and feeding deterrent activity of ten compounds occurring commonly in essential oils was explored in order to determine whether they are acute toxins or antifeedants against stored-grain pests. Simultaneously, the objective was also to demonstrate the comparative efficacy against three post-harvest stored-grain pests. Thymol, carvacrol, eugenol and trans-anethole were specifically toxic, and linalool was a generalist feeding deterrent against all three species studied. Thymol was most toxic to Tribolium castaneum and Rhyzopertha dominica compared to carvacrol and eugenol but was least toxic to Sitophilus oryzae. Similarly, linalool deterred feeding of S. oryzae (FI50 = 0.025 mg/g of the wafer diet), T. castaneum (FI50 = 0.207 mg/g of the wafer diet) and R. dominica (FI50 = 0.482 mg/g of the wafer diet) at different concentrations; R. dominica beetles required about 20 times the concentration to deter feeding compared to S. oryzae and more than twice compared to T. castaneum. Comparison of toxicity and deterrent activity with respective artificial blends as binary mixtures revealed that synergism was not a generalized phenomenon, and the variations were both species as well as blend specific. Individual compound efficacy correlations were not ascertained, which suggests that artificial blends could be prepared to obtain potential mixtures for substantial control of stored-grain insect pests. The present study also implies that the compounds are mostly acute toxins, and whatever inhibition in feeding was obtained could be due to physiological toxicity rather than any interaction with gustatory receptors.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abdelgaleil SAM, Mohamed MIE, Badawy MEI, El-arami SAA (2009) Fumigant and contact toxicities of monoterpenes to Sitophilus oryzae (L.) and Tribolium castaneum (Herbst.) and their inhibitory effects on acetylcholinesterase activity. J Chem Ecol 35:518–525

    Article  CAS  PubMed  Google Scholar 

  • Abdelgaleil SAM, Mohamed MIE, Shawir MS, Abou-Taleb HK (2016) Chemical composition, insecticidal and biochemical effects of essential oils of different plant species from Northern Egypt on the rice weevil, Sitophilus oryzae L. J Pest Sci 89:219–229

    Article  Google Scholar 

  • Akhtar Y, Pages E, Styevens A, Bradbury R, daCamara CAG, Isman MB (2012) Effect of chemical complexity of essential oils on feeding deterrence in larvae of the cabbage looper. Physiol Entomol 37:81–91

    Article  CAS  Google Scholar 

  • Al-reza SM, Rahman A, Ahmad Y, Chul S (2010) Inhibition of plant pathogens in vitro and in vivo with essential oils and organic extracts of Cestrum nocturnum L. Pestic Biochem Physiol 96:86–92

    Article  CAS  Google Scholar 

  • Anonymous (1997) Parties of the Montreal protocol on substances that deplete the ozone layer, Montreal, Canada

  • Bedini S, Flamini G, Girardi J, Cosci F, Conti B (2015) Not just for beer: evaluation of spent hops (Humulus lupulus L.) as a source of eco-friendly repellents for insect pests of stored foods. J Pest Sci 88:583–592

    Article  Google Scholar 

  • Bischof LJ, Enan EE (2004) Cloning, expression and functional analysis of an octopamine receptor from Periplaneta americana. Insect Biochem Mol Biol 34:511–521

    Article  CAS  PubMed  Google Scholar 

  • Boxall RA (1991) Post-harvest losses to insects—a world overview. In: Rossmoore HW (ed) Biodeterioration and biodegradation, vol 8. Elsevier Applied Science, London, pp 160–175

    Google Scholar 

  • Buckle J (2003) Clinical aromatherapy: essential oils in practice. Churchill Livingstone, Edinburgh

    Google Scholar 

  • Coppen JJW (1995) Flavours and fragrances of plant origin. Food and Agricultural Organization, Rome

    Google Scholar 

  • Enan EE (2001) Insecticidal activity of essential oils: octopaminergic sites of action. Comp Biochem Physiol 130:325–327

    CAS  Google Scholar 

  • Enan EE (2005) Molecμar response of Drosophila melanogaster tyramine receptor cascade to plant essential oils. Insect Biochem Mol Biol 35:309–321

    Article  CAS  PubMed  Google Scholar 

  • Environmental Protection Agency, EPA (1993) Regulatory action under the clean air act on methyl bromide. United States Environmental Protection Agency, Office of Air Radiation, Strategic Protection Division, Washington, DC

  • Finney DJ (1971) Probit analysis. Cambridge University Press, Cambridge, 350 pp

  • Garry VF, Griffth J, Danzl TJ, Nelson RL, Whorton EB, Krueger LA, Cervenka J (1989) Human genotoxicity: pesticide applicators and phosphine. Science 246:251–255

    Article  CAS  PubMed  Google Scholar 

  • Garry VF, Nelson RL, Griffth J, Harkins M (1990) Preparation for human study of pesticide applicators: sister chromatid exchanges and chromosome aberrations in cultured human lymphocytes exposed to selected fumigants. Teratog Carcinog Mutagen 10:21–29

    Article  CAS  PubMed  Google Scholar 

  • Germinara GS, De Cristofaro A, Rotundo G (2015) Repellents effectively disrupt the olfactory orientation of Sitophilus granarius to wheat kernels. J Pest Sci 88:675–684

    Article  Google Scholar 

  • Gorham JR (1991) Ecology and Management of Food-Industry Pests. Association of Official Analytical Chemists, Arlington

    Google Scholar 

  • Ho SH, Ma Y, Huang Y (1997) Anethole, a potential insecticide from Illicium verum Hook F. against two stored product insects. Int J Pest Cont 39:50–51

    CAS  Google Scholar 

  • Huang Y, Ho SH (1998) Toxicity and antifeedant activity of cinnamaldehyde against the grain storage insects, Tribolium castaneum (Herbst) and Sitophilus zeamais Motsch. J Stored Prod Res 34:11–17

    Article  CAS  Google Scholar 

  • Huang Y, Chen SX, Ho SH (2000) Bioactivities of methyl allyl disulfide and diallyl trisulfide from essential oil of garlic to two species of stored product pests, Sitophilus zeamais (Coleoptera: Curculionidae) and Tribolium castaneum (Coleoptera: Tenebrionidae). J Econ Entomol 93:537–543

    Article  CAS  PubMed  Google Scholar 

  • Hummelbrunner LA, Isman MB (2001) Acute, sublethal, antifeedant, and synergistic effects of monoterpenoid essential oil compounds on the tobacco cutworm, Spodoptera litura (Lep., Noctuidae). J Agric Food Chem 49:715–720

    Article  CAS  PubMed  Google Scholar 

  • Hymavathi A, Devanand P, Suresh Babu K, Sreelatha T, Pathipati UR, Madhusudana Rao J (2011) Vapor-phase toxicity of Derris scandens Benth.-derived constituents against four stored-product pests. J Agric Food Chem 59:1653–1657

    Article  CAS  PubMed  Google Scholar 

  • Isman MB (2000) Plant essential oils for pest and disease management. Crop Prot 19:603–608

    Article  CAS  Google Scholar 

  • Karr I, Coats RJ (1988) Insecticidal properties of d-limonene. J Pestic Sci 13:287–290

    Article  CAS  Google Scholar 

  • Kim S-I, Roh J-Y, Kim D-H, Lee H-S, Ahn Y-J (2003) Insecticidal activities of aromatic plant extracts and essential oils against Sitophilus oryzae and Callosobruchus chinensis. J Stored Prod Res 39:293–303

    Article  CAS  Google Scholar 

  • Kim S-W, Lee H-R, Jang M-J, Jung C-S, Park I-K (2016) Fumigant toxicity of Lamiaceae plant essential oil and blends of their constituents against rice weevil, Sitophilus oryzae. Molecules 21:361. doi:10.3390/molecules21030361

    Article  PubMed  Google Scholar 

  • Kostyukovsky M, Rafaeli A, Gileadi C, Demchenko N, Shaaya E (2002) Activation of octopaminergic receptors by essential oil constituent isolated from aromatic plants: possible mode of action against insect pests. Pest Manag Sci 58:1101–1106

    Article  CAS  PubMed  Google Scholar 

  • Koul O (2004) Bioactivity of volatile di-n-propyl disulfide from seeds of neem, Azadirachta indica (Meliaceae) to two species of stored grain pests, Sitophilus oryzae (L.) and Tribolium castaneum (Herbst). J Econ Entomol 97:1142–1147

    Article  CAS  PubMed  Google Scholar 

  • Koul O (2005) Insect antifeedants. CRC Press, Boca Raton

    Google Scholar 

  • Koul O (2008) Phytochemicals and insect control: an antifeedant approach. Crit Rev Plant Sci 27:1–24

    Article  CAS  Google Scholar 

  • Koul O (2012) Plant biodiversity as a resource for natural products for insect pest management. In: Gurr GM, Wratten SD, Snyder WE, Read DMY (eds) Biodiversity and insect pests: key issues for sustainable management. Wiley, Australia, pp 85–105

    Chapter  Google Scholar 

  • Koul O, Singh G, Singh R, Singh J (2007) Mortality and reproductive performance of Triboilum castaneum exposed to anethole vapours at high temperature. Biopestic Int 3:126–137

    Google Scholar 

  • Koul O, Walia S, Dhaliwal GS (2008) Essential oils as green pesticides: potential and constraints. Biopestic Int 4:63–84

    Google Scholar 

  • Koul O, Singh R, Kaur B, Kanda D (2013) Comparative study on the behavioral response and acute toxicity of some essential oil compounds and their binary mixtures to larvae of Helicoverpa armigera, Spodoptera litura and Chilo partellus. Indus Crops Prod 49:428–436

    Article  CAS  Google Scholar 

  • Kumrungsee N, Pluempanupat W, Koul O, Bullangpoti V (2014) Toxicity of essential oil compounds against diamondback moth, Plutella xylostella, and their impact on detoxification enzyme activities. J Pest Sci 87:721–729

    Article  Google Scholar 

  • Lee BH, Choi WS, Lee SE, Park BS (2001a) Fumigant toxicity of essential oils and their constituent compounds towards the rice weevil, Sitophilus oryzae (L.). Crop Prot 20:317–320

    Article  CAS  Google Scholar 

  • Lee SE, Lee BH, Choi WS, Park BS, Kim JG, Campbell BC (2001b) Fumigant toxicity of volatile natural products from Korean spices and medicinal plants towards the rice weevil, Sitophilus oryzae (L). Pest Manag Sci 57:548–553

    Article  CAS  PubMed  Google Scholar 

  • Makhijani A, Gurney KR (1995) Mending the ozone hole: science, technology and policy. MIT Press, Cambridge

    Google Scholar 

  • Mason LJ, McDonough JA (2012) Biology, behavior and ecology of stored grain and legume insects. In: Hagstrum DW, Phillips TW, Cuperus GW (eds) Stored product protection. Kansas State University, Manhatan, pp 7–20

    Google Scholar 

  • Mordue (Luntz) AJ (2004) Present concepts of the mode of action of azadirachtin from neem. In: Koul O, Wahab S (eds) Neem today and in the new millennium. Kluwer Academic Press, Dordrecht, pp 229–242

    Chapter  Google Scholar 

  • Nawrot J, Harmatha J (2012) Phytochemical feeding deterrents for stored product insect pests. Phytochem Rev 11:543–566

    Article  CAS  Google Scholar 

  • Park CG, Shin E, Kim J (2016) Insecticidal activities of essential oils, Gaultheria fragrantissima and Illicium verum, their components and analogs against Callosobruchus chinensis adults. J Asia Pacific Entomol 19:269–273

    Article  CAS  Google Scholar 

  • Paruch E, Ciunik Z, Nawrot J, Wawrzencyzk C (2000) Lactones. 9. Synthesis of terpenoid lactones: active insect antifeedants. J Agric Food Chem 48:4973–4977

    Article  CAS  PubMed  Google Scholar 

  • Pavela R (2014) Acute, synergistic and antagonistic effects of some aromatic compounds on the Spodoptera littoralis Boisd (Lepidoptera: Noctuidae) larvae. Indus Crops Prod 60:247–258

    Article  CAS  Google Scholar 

  • Pavela R (2015) Acute toxicity and synergistic and antagonistic effects of the aromatic compounds of some essential oils against Culex quinquefasciatus Say larvae. Parasitol Res 114:3835–3853

    Article  PubMed  Google Scholar 

  • Phillips TW, Throne JE (2010) Biorational approaches to managing stored product insects. Annu Rev Entomol 55:375–397

    Article  CAS  PubMed  Google Scholar 

  • Priestley CM, Williamson EM, Wafford KA, Satelle DB (2003) Thymol, a constituent of thyme essential oils, is a positive modulator of human GABA and a homo-oligosteric GABA receptor from Drosophila melanogaster. Brit J Pharmacol 140:1363–1367

    Article  CAS  Google Scholar 

  • Rajendran S (2016) Status of fumigation in stored grains in India. Indian J Entomol 78:28–38

    Article  Google Scholar 

  • Regnault-Roger C, Vincent C, Arnason JT (2012) Essential oils and insect control: low-risk products in a high-stakes world. Annu Rev Entomol 57:405–424

    Article  CAS  PubMed  Google Scholar 

  • Rice ND, Winston ML, Whittington R, Higo HA (2002) Comparison of release mechanisms for botanical oils to control Varroa destructor (Acari: Varroidae) and Acarapis woodi (Acari: Tarsonemidae) in colonies of honey bees (Hymenoptera: Apidae). J Econ Entomol 95:221–226

    Article  CAS  PubMed  Google Scholar 

  • Rozman V, Kalinovic I, Korunic Z (2007) Toxicity of naturally occurring compounds of Lamiaceae and Lauraceae to three stored product insects. J Stored Prod Res 43:349–355

    Article  CAS  Google Scholar 

  • Sarac A, Tunc I (1995) Toxicity of essential oil vapours to stored-product insects. J Plant Dis Prot 102:69–74

    CAS  Google Scholar 

  • Scott IM, Puniani E, Durst T, Phelps D, Merali S, Assabgui RA, Sánchez-Vindas P, Poveda L, Philogène BJR, Arnason JT (2002) Insecticidal activity of Piper tuberculatum Jacq. extracts: synergistic interaction of piperamides. Agric Forest Entomol 4:137–144

    Article  Google Scholar 

  • Shaaya E, Ravid U, Paster N, Juven B, Zisman U, Pissarev V (1991) Fumigant toxicity of essential oils against four major stored-product insects. J Chem Ecol 17:499–504

    Article  CAS  PubMed  Google Scholar 

  • Shaaya E, Kostjukovsky M, Ravid U (1994) Essential oils and their constituents as effective fumigants against stored product insects. Israel Agres 7:133–139

    Google Scholar 

  • Stroh J, Wan MT, Isman MB, Moul DJ (1998) Evaluation of the acute toxicity to juvenile Pacific coho salmon and rainbow trout of some plant essential oils, a formulated product, and the carrier. Bull Environ Contam Toxicol 60:923–930

    Article  CAS  PubMed  Google Scholar 

  • Tak J-H, Isman MB (2015) Enhanced cuticular penetration as the mechanism for synergy of insecticidal constituents of rosemary essential oil in Trichoplusia ni. Sci Rep. doi:10.1038/srep12690

    Google Scholar 

  • Tak J-H, Jovel E, Isman MB (2015) Comparative and synergistic activity of Rosmarinus officinalis L. essential oil constituents against the larvae and an ovarian cell line of the cabbage looper, Trichoplusia ni (Lepidoptera: Noctuidae). Pest Manag Sci 72:474–480

    Article  PubMed  Google Scholar 

  • Tripathi AK, Prajapati V, Kumar S (2003) Bioactivities of l-carvone, d-carvone, and dihydrocarvone towards three stored product beetles. J Econ Entomol 96:1594–1601

    Article  CAS  PubMed  Google Scholar 

  • Trisyono A, Whalon M (1999) Toxicity of neem applied alone and in combinations with Bacillus thuringiensis to Colorado potato beetle (Coleoptera: Chrysomelidae). J Econ Entomol 92:1281–1288

    Article  CAS  Google Scholar 

  • Trumble JT (2002) Caveat emptor: safety considerations for natural products used in pest control. Am Entomol 48:7–13

    Article  Google Scholar 

  • Wang Y, You CX, Yang K, Wu Y, Chen R, Zhang WJ, Liu ZL, Du SS, Deng ZW, Geng ZF, Han J (2015) Bioactivity of essential oil of Zingiber purpureum rhizomes and its main compounds against two stored product insects. J Econ Entomol 108:925–932

    Article  CAS  PubMed  Google Scholar 

  • Weaver DK, Dunkel FV, Ntezurubaza L, Jackson LL, Stock DT (1991) The efficacy of linalool a major component of freshly milled Ocimum canum Sims (Lamiaceae) for protection against post-harvest damage by certain stored product Coleoptera. J Stored Prod Res 27:213–220

    Article  CAS  Google Scholar 

  • Wilson JA, Isman MB (2006) Influence of essential oils on toxicity and pharmacokinetics of the plant toxin thymol in the larvae of Trichoplusia ni. Can Entomol 138:578–589

    Article  Google Scholar 

  • Yildirim E, Emsen B, Kordali S (2013) Insecticidal effects of monoterpenes on Sitophilus zeamais Motschulsky (Coleoptera: Curculionidae). J Appl Bot Food Qual 86:198–204

    CAS  Google Scholar 

  • Zettler JL (1991) Pesticide resistance in Tribolium castaneum and T. confusum (Coleoptera: Tenebrionidae) from flour mills in the United States. J Econ Entomol 84:763–767

    Article  Google Scholar 

Download references

Acknowledgments

Authors are thankful to Prof. M. B. Isman, University of British Columbia, Vancouver, Canada, and his group for valuable comments on the earlier version of this paper.

Author information

Authors and Affiliations

  1. Insect Biopesticide Research Centre, 30 Parkash Nagar, Jalandhar, 144003, India

    Dharamvir Kanda & Opender Koul

  2. Department of Zoology, Guru Nanak Dev University, Amritsar, 143005, India

    Sanehdeep Kaur

Authors
  1. Dharamvir Kanda
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sanehdeep Kaur
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Opender Koul
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Opender Koul.

Ethics declarations

Conflict of interest

The authors, DK, SK and OK, declare that they have no conflict of interests.

Funding

This study was supported by the routine internal funds of the Insect Biopesticide Research Centre, Jalandhar, India.

Human and animal research information

This article does not contain any studies with human participants performed by any of the authors. All applicable international, national and/or institutional guidelines for the care and use of insects were followed.

Additional information

Communicated by M. B. Isman.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kanda, D., Kaur, S. & Koul, O. A comparative study of monoterpenoids and phenylpropanoids from essential oils against stored grain insects: acute toxins or feeding deterrents. J Pest Sci 90, 531–545 (2017). https://doi.org/10.1007/s10340-016-0800-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10340-016-0800-5

Keywords

Search

Navigation