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ISSN : 1225-0171(Print)
ISSN : 2287-545X(Online)
Korean Journal of Applied Entomology Vol.56 No.4 pp.395-402

Essential Oil Isolated from Iranian Yarrow as a Bio-rational Agent to the Management of Saw-toothed Grain Beetle, Oryzaephilus surinamensis (L.)

Asgar Ebadollahi*
이란 아르다빌리 모하그 대학교, 농업자연자원대학(모그한 캠퍼스)
Corresponding author:
09/09/2017 05/11/2017 09/11/2017


Overuse of synthetic pesticides caused negative side-effects such as environmental contamination, development of insect pests’ resistance, and effects on non-target organisms. Plant origin substances without/or with low mammalian toxicity have been considered as promising alternatives to the synthetic pesticides. Fumigant toxicity of the essential oil of Iranian Yarrow, Achillea millefolium L., was investigated against a cosmopolitan stored-product insect pest: saw-toothed grain beetle (Oryzaephilus surinamensis L.). Chemical profile of this essential oil was studied by Gas Chromatography-Mass Spectrometry. Tested concentrations were significantly effective to the mortality of insect pest. A positive correlation between essential oil concentrations and pest mortality were realized. LC50 value (lethal concentration needed to 50% mortality) was achieved as 17.977 (16.195 ± 20.433) μl/l air. The main components were 1,8-Cineole (13.17%), nerolidol (12.87%), α-cubebene (12.35%), artemisia ketone (6.69%), α-terpineol (5.27%), alloaromadendrene oxide (4.71%) and borneol (3.99%). Terpenic compounds including monoterpene hydrocarbons (8.19%), monoterpenoids (44.23%), sesquiterpene hydrocarbons (21.69%) and sesquiterpenoids (22.24%) were 96.35% of the total identified compounds. Results indicated that the terpene-rich A. millefolium essential oil may be considered as a safe bio-agent in the O. surinamensis management.

머리대장가는납작벌레의 합리적 방제 물질로 이란 서양가새풀 정유의 살충효과 평가

아 스가르 에바돌라히*
Moghan College of Agriculture and Natural Resources, University of Mohaghegh Ardabili, Ardabil, Iran


유기합성 농약의 과다사용은 환경오염, 살충제 저항성 발달, 비표적 생물에 대한 영향 등 부작용의 원인이 되고 있다. 유기합성 농약의 대체약 제로 포유동물에 저독성인 식물기원 물질이 각광을 받게 되었다. 이란 서양가새풀(Achillea millefolium L.) 정유성분의 훈증독성은 국제적 저장작 물 해충인 머리대장가는납작벌레(Oryzaephilus surinamensis L.)의 방제제로 연구된 바 있다. 이 식물 정유의 화학적 성분을 가스크로마트 그래피 (MS)를 이용하여 분석하였다. 살충실험 결과 처리농도에 따라 유의한 살충률을 나타냈다. 처리농도와 살충률 간 양의 상관관계가 있었다. 반치사 농도(LC50)는 17.977 μl/L 이었다. 주요 성분은 1,8-Cineole (13.17%), nerolidol (12.87%), α-cubebene (12.35%), artemisia ketone (6.69%), α-terpineol (5.27%), alloaromadendrene oxide (4.71%) 및 borneol (3.99%) 이었다. 전체 동정된 화합물의 96.35%는 Terpenic 화합물로 monoterpene hydrocarbons (8.19%), monoterpenoids (44.23%), sesquiterpene hydrocarbons (21.69%) 및 sesquiterpenoids (22.24%)를 포함하고 있었다. 본 결과는 terpene이 풍부한 서양가새풀 정유가 머리대장가는납작벌레의 안전한 생물농약으로 고려될 수 있음을 보여주었다.

    University of Mohaghegh Ardabili, Ardabil, Iran.

    Saw-toothed grain beetle (Oryzaephilus surinamensis L.) as one of the cosmopolitan insect pest of processed and packaged commodities, can attack many stored-products including cereals, dried fruit and oilseeds. The larvae and adults are external feeders and are very active. It has a worldwide distribution even in cold areas (Rees, 2007). The life cycle of this pest can be completed within 20 days at 33℃ and 80% relative humidity (Beckel et al., 2007).

    The utilization of some chemicals such as sulfuryl fluoride, methyl bromide and phosphine has been developed for management of stored-product insect pests but their abuse has resulted in negative side-effects such as threat to non-target organisms and environmental contamination (Jeyasankar and Jesudasan, 2005; Damalas and Eleftherohorinos, 2011; Carvalho, 2017). Further, there are several documents related to the resistance of stored product pests including O. surinamensis to the phosphine and some other chemical fumigants (Daglish, 2004; Collins et al., 2005; Pimentel et al., 2008). Therefore, search for safe and eco-friendly pesticides is necessary.

    Plant essential oils, with low persistence in the environment, have several volatile compounds such as terpenic and aromatic constituents (Bakkali et al., 2008) and their toxicity to the mammals is low (Cloyd et al., 2009; El Asbahani et al., 2015). Recent studies indicated that they are effective against different orders of pests and can be considered as safe and available bio-pesticides (Isman and Grieneisen, 2014; Ebadollahi and Jalali-Sendi, 2015).

    Achillea species from Asteraceae family with aromatic leaves and flowers become globally known medicinal herbs and subjected to numerous pharmacological and biological studies (Nemeth, 2005; Nemeth and Bernath, 2008). Yarrow, A. millefolium L., has been showed significance pharmacological activities and become a most important among Achillea species (Csupor-Loffler et al., 2009; Saeidnia et al., 2011; Demirci et al., 2017).

    Susceptibility of O. surinamensis to the essential oils was considered in the recent researches, in which the essential oils of Agastache foeniculum (Pursh) Kuntze (Ebadollahi et al., 2010), Artemisia argyi Levl et Vant (Lü et al., 2011), Eucalyptus dundasii Maiden (Parsia-Aref et al., 2015), and Ocimum gratissimum L. (Ogendo et al., 2008) presented significant toxicity. Based on the ongoing world-wide researches to the screening of plant-derived agents, the main objective was to assess the insecticidal effect of essential oil isolated from Iranian A. millefolium against O. surinamensis. Further, evaluation of the chemical composition of this oil was the other aim.

    Materials and Methods

    Essential oil extraction and analysis

    Aerial parts of A. millefolium were collected from Sardabeh county, Ardabil province, Iran. Flowers were separated after air-drying at room temperature (27 ± 2℃) in 10 days. Samples were crushed into powder using an electric grinder and were hydro-distilled using a Clevenger apparatus. Essential oil extraction conditions were: 100 g plant material, 2000 ml distilled water and 180 min distillation period.

    The chemical components of essential oil isolated from A. millefolium was investigated by a Hewlett-Packard Gas Chromatography (HP, Palo Alto, CA) equipped with a mass sensitive detector (5975C) according to the our recent study: Ebadollahi et al (2017). Identification was made through comparison of their patterns and coincidence fragmentation with the standard spectra present in the library of the instrument (Adams, 2004): Wiley 7n.1 mass computer library and NIST (National Institute of Standards and Technology).

    Rearing of insect pest

    Parent adults of Oryzaephilus surinamensis were collected from contaminated rice grains of Ardabil city, Iran. It was reared in 1-liter glass containers comprising the wheat flour. Containers were covered with a mesh cloth for ventilation. Adult insects with 1-3 days old were used for bioassays. Insects were kept in the dark in an incubator set at 27 ± 2˚C and 65 ± 5% Relative Humidity.

    Insecticidal activity

    Based on a preliminary experiment, concentrations of 13.33, 15.23, 17.37, 19.85 and 22.67 μl/l air were selected for evaluation of the toxicity of A. millefolium essential oil on the adults of O. surinamensis. Required concentrations were poured on 2 × 3 cm filter papers (Whatman No. 1) which were positioned at the bottom of 750 ml glass containers. Twenty adult insects (1-3 days old) were located in the 3.5 × 5 cm tubes covered with cloth mesh. In general, 120 adults’ insects were used for each replication. Tubes were then hung at the midpoint of containers and air-tightly closed. The same procedures were considered for control groups without oil concentrations. Four replications were made and the insect mortality was determined after 24 h exposure time.

    Statistical analysis

    Data were analyzed by ANOVA (analysis of variance) with SPSS software (Version 16) and differences were confirmed by the results of Tukey’s test at P < 0.05. Lethal concentrations were calculated through Probit analysis and linear regression analysis was accomplished to designate insect mortality in contradiction of oil concentrations.


    Chemical composition of essential oil

    Chemical components of A. millefolium essential oil are shown in Fig. 1 and Table 1. Sixty-two components representing 99.81% of the total oil were recognized, in which 1,8-Cineole (13.17%), nerolidol (12.87%), α-cubebene (12.35%), artemisia ketone (6.69%), α-terpineol (5.27%), alloaromadendrene oxide (4.71%) and borneol (3.99%) were the main components. Terpenic compounds including monoterpene hydrocarbons (8.19%), monoterpenoids (44.23%), sesquiterpene hydrocarbons (21.69%) and sesquiterpenoids (22.24%) were 96.35% of the total identified compounds (Fig. 1 and Table 1).

    Insecticidal activity

    Essential oil isolated from an aerial part of A. millefolium had strong fumigant toxicity against O. surinamensis. Analysis of variance revealed tested concentrations were meaningfully toxic to the pest (F = 156.689, df = 4, 15 and P < 0.0001). There wasn’t any mortality in the control groups. Created mortalities through all essential oil concentrations were taken different letters by Turkey’s test at P = 0.05 (Fig. 2).

    According to R2 value in Table 2, a positive correlation between essential oil concentrations and mortality of the pest was recognized. LC50 was calculated as 17.977 (16.195 ± 20.433) μl/l air (Table 2).


    The chemical composition of A. millefolium essential oil was investigated in recent studies. For example, Orav et al. (2006) indicated that some terpenic components including sabinene, β-pinene, 1,8-cineole, artemisia ketone, and linalool were the main components in A. millefolium essential oils from some European countries. Some of these compounds such as sabinene, 1,8-cineole, and artemisia ketone were also recognized in this study. Orav et al. (2006) were also showed that samples from Estonia, Hungary, and Greek contained high amounts of Monoterpene hydrocarbons, and essential oils from France, Belgium and Russia were rich in oxygenated monoterpenes. They also realized the essential oils from Greece, Estonia and Moldavia were rich in sesquiterpenes. According to results of our study, Iranian A. millefolium essential oil was rich in terpenic compounds (96.35%) in which monoterpenoids (44.23%) has high amount. Nadim et al. (2011) showed that borneol, bornyl acetate, 1,8-cineole, α-pinene, β-pinene, sabinene, and terpinine-4-ol had high amount in the A. mellifolium essential oil from India. Some of these compounds were also recognized in the present study but with some quantitative differences. For example, sabinene, 1,8-cineole and bornyl acetate were 17.58%, 13.04% and 7.98% in the study of Nadim et al. (2011) but these compounds respectively were 2.78%, 13.17% and 0.58% in the present work. Therefore, there are differences in the kind and quantity of the components between previous reports and the results of present study. The differences may be due to a number of endogenous (genetic makeup and plant stages) and exogenous factors (method of essential oil extraction and geographical position) which affect composition of essential oils (Ozguven et al., 2008; Ben Jemâa et al., 2012; Khanavi et al., 2013; Zandi-Sohani and Ramezani, 2015).

    Although pesticidal activity of Achillea essential oils was evaluated against some economical pests (Calmasur et al., 2006; Rafiei Karahroodi et al., 2009; Dehghani and Ahmadi, 2013), the toxic effect of A. millefolium essential oil was tested against O. surinamensis for first time in this work. Moreover, the toxicity of some terpenic components was investigated against some insect pests by previous researchers. For example, fumigant toxicity of 20 naturally occurring monoterpenoids was assessed against O. surinamensis and it was found that 1,8-cineole and terpineol produced 100% mortality at 50 mg/ml air (Lee et al., 2003). In the other studies, fumigant toxicity of some terpenic compounds including 1,8-cineole, camphor, eugenol, linalool, carvacrol, thymol, borneol, and bornyl-acetate was evaluated against major stored-product insect pests: Sitophilus oryzae L., Rhyzopertha dominica F. and Tribolium castaneum Herbst (Rozman et al., 2007). Nerolidol was also showed considerable toxicity (LD50 = 29.30 μg/adult) against Sitophilus zeamais Motsch (Yang et al., 2011). Consequently, the toxicity of A. millefolium essential oil may be related to the bioactive constituents such as 1,8-cineole, nerolidol, terpineol and borneol.

    Plant essential oils have been known as secondary metabolites in the chemical defense mechanisms towards aggressive organisms such as arthropod pests (Prakash and Rao, 1997). Essential oils contain evolutionary origin complex of chemical constituents which are responsible for their bio-activities. For this reason, pests’ resistance to these materials will be low (Isman, 2006). They are also considered as safe and available bio-rational agents in insect pests’ management (Regnault- Roger et al., 2012). The essential oil of A. millefolium indicated promising toxicity against O. surinamensis, in the present study. Based on the results of present and previous works, the essential oil of A. millefolium is useful in the management of O. surinamensis. However, additional researches are needed to achievement of new practical formulations and cost reduction.


    This project was supported by the University of Mohaghegh Ardabili, Ardabil, Iran.


    GC-MS chromatogram of the essential oil isolated from Achillea millefolium.


    Mean mortality of O. surinamensis affected by the different concentrations of A. millefolium essential oil. Dissimilar letters display significant differences based on Tukey test at p < 0.05. Vertical bars show standard error (±).

    Chemical composition of essential of Iranian Achillea millefolium

    Results of Probit analysis of fumigant toxicity of essential oil isolated from A. millefolium against O. surinamensis


    1. Adams R.P. (2004) Identification of essential oil component by gas chromatography/ Quadrupole Mass spectroscopy., Allured Publishing Corporation,
    2. Bakkali F. , Averbeck S. , Averbeck D. , Idaomar M. (2008) Biological effects of essential oils - a review. , Food Chem. Toxicol., Vol.46 ; pp.446-475
    3. Beckel H.S. , Lorini I. , Lazzari S.M. (2007) Rearing method of Oryzaephilus surinamensis (L.) (Coleoptera, Silvanidae) on various wheat grain granulometry. , Rev. Bras. Entomol., Vol.51 (4) ; pp.501-505
    4. Ben JemA a J.M. , Haoue S. , Bouaziz M. , Khouja M.L. (2012) Seasonal variations in chemical composition and fumigant activity of five Eucalyptus essential oils against three moth pests of stored dates in Tunisia. , J. Stored Prod. Res., Vol.48 ; pp.61-67
    5. Calmasur O. , Kordali S. , Kaya O. , Aslan I. (2006) Toxicity of essential oil vapours obtained from Achillea spp. to Sitophilus granarius (L.) and Tribolium confusum (Jacquelin du Val). , J. Plant Dis. Prot., Vol.113 (1) ; pp.37-41
    6. Carvalho F.P. (2017) Pesticides, environment, and food safety. , Food Energy Secur., Vol.6 (2) ; pp.48-60
    7. Cloyd R.A. , Galle C.L. , Keith S.R. , Kalscheur N.A. , Kemp K.E. (2009) Effect of commercially available plant derived essential oil products on arthropod pests. , J. Econ. Entomol., Vol.102 ; pp.1567-1579
    8. Collins P.J. , Daglish G.J. , Pavic H. , Kopittke R.A. (2005) Response of mixed-age cultures of phosphine-resistant and susceptible strains of lesser grain borer, Rhyzopertha dominica, to phosphine at a range of concentrations and exposure periods. , J. Stored Prod. Res., Vol.41 ; pp.373-385
    9. Csupor-Loffler B. , Hajdu Z. , Zupko I. , Rethy B. , Falkay G. , Forgo P. , Hohmann J. (2009) Antiproliferative effect of flavonoids and sesquiterpenoids from Achillea millefolium L. on cultured human tumour cell lines. , Phytother. Res., Vol.23 (5) ; pp.672-676
    10. Daglish G.J. (2004) Effect of exposure period on degree of dominance of phosphine resistance in adults of Rhyzopertha dominica (Coleoptera: Bostrichidae) and Sitophilus oryzae (Coleoptera: Curculionidae). , Pest Manag. Sci., Vol.60 ; pp.822-826
    11. Damalas C.A. , Eleftherohorinos I.G. (2011) Pesticide Exposure, Safety Issues, and Risk Assessment Indicators. , Int. J. Environ. Res. Public Health, Vol.8 ; pp.1402-1419
    12. Dehghani M. , Ahmadi K. (2013) Anti-oviposition and repellence activities of essential oils and aqueous extracts from five aromatic plants against greenhouse whitefly Trialeurodes vaporariorum Westwood (Homoptera: Aleyrodidae). , Bulg. J. Agric. Sci., Vol.19 ; pp.691-696
    13. Demirci B. , Can Başer K.H. , Aytaç Z. , Khan S.I. , Jacob M.R. , Tabanca N. (2017) Comparative study of three Achillea essentialoils from eastern part of Turkey and their biological activities. , Rec. Nat. Prod.,
    14. Ebadollahi A. , Jalali Sendi J. , Aliakbar A. (2017) Efficacy of nanoencapsulated Thymus eriocalyx and Thymus kotschyanus essential oils by a mesoporous material MCM-41 against Tetranychus urticae (Acari: Tetranychidae). , J. Econ. Entomol.,
    15. Ebadollahi A. , Jalali-Sendi J. (2015) A review on recent research results on bio-effects of plant essential oils against major Coleopteran insect pests. , Toxin Rev., Vol.34 (2) ; pp.76-91
    16. Ebadollahi A. , Safaralizadeh M.H. , Pourmirza A.A. , Gheibi S.A. (2010) Toxicity of essential oil of Agastache foeniculum (Pursh) Kuntze to Oryzaephilus surinamensis L. and Lasioderma serricorne F. , J. Plant Prot. Res., Vol.50 (2) ; pp.215-219
    17. El Asbahani A. , Miladi K. , Badri W. , Sala M. , AA_t Addi E.H. , Casabianca H. , El Mousadik A. , Hartmann D. , Jilale A. , Renaud F.N. , Elaissari A. (2015) Essential oils: From extraction to encapsulation. , Int. J. Pharm., Vol.483 (1-2) ; pp.220-243
    18. Isman M.B. (2006) Botanical insecticides, deterrents, and repellents in modern agriculture and an increasingly regulated world. , Annu. Rev. Entomol., Vol.51 ; pp.45-66
    19. Isman M.B. , Grieneisen M.L. (2014) Botanical insecticide research: many publications, limited useful data. , Trends Plant Sci., Vol.19 ; pp.140-145
    20. Jeyasankar A. , Jesudasan R.W. (2005) Insecticidal properties of novel botanicals against a few lepidopteran pests. , Pestology, Vol.29 ; pp.42-44
    21. Khanavi M. , Hajimehdipoor H. , Emadi F. , Kalantari Khandani N. (2013) Essential oil compositions of Thymus kotschyanus Boiss. obtained by hydrodistillation and microwave oven distillation. , J.Essent. Oil Bear. Plants, Vol.16 ; pp.117-122
    22. Lee S. , Peterson C.J. , Coats J.R. (2003) Fumigation toxicity of monoterpenoids to several stored product insects. , J. Stored Prod. Res., Vol.39 ; pp.77-85
    23. LA1/4 J. , Wu C. , Shi Y. (2011) Toxicity of essential oil from Artemisia argyi against Oryzaephilus surinamensis (Linnaeus) (Coleoptera: Silvanidae). , Afr. J. Microbiol. Res., Vol.5 (18) ; pp.2816-2819
    24. Nadim M.M. , Malik A.A. , Ahmad J. , Bakshi S.K. (2011) The essential oil composition of Achillea millefolium L. cultivated under tropical condition in India. , World J. Agric. Sci., Vol.7 (5) ; pp.561-565
    25. Nemeth E. (2005) Essential oil composition of species in the genus Achillea. , J. Essent. Oil Res., Vol.17 (5) ; pp.501-512
    26. Nemeth E. , Bernath J. (2008) Biological activities of Yarrow Species (Achillea spp.). , Curr. Pharm. Des., Vol.14 ; pp.3151-3167
    27. Ogendo J.O. , Kostyukovsky M. , Ravid U. , Matasyoh J.C. , Deng A.L. , Omolo E.O. , Kariuki S.T. , Shaaya E. (2008) Bioactivity ofOcimum gratissimum L. oil and two of its constituents against five insect pests attacking stored food products. , J. Stored Prod. Res., Vol.44 ; pp.328-334
    28. Orav A. , Arak E. , Raal A. (2006) Phytochemical analysis of the essential oil of Achillea millefolium L. from various Europeancountries. , Nat. Prod. Res., Vol.20 (12) ; pp.1082-1088
    29. Ozguven M. , Sener B. , Orhan I. , Sekeroglu N. , Kirpik M. , Kartal M. , Pesin I. , Kaya Z. (2008) Effects of varying nitrogen doses on yield, yield components and artemisinin content of Artemisia annua L. , Ind. Crops Prod., Vol.27 ; pp.60-64
    30. Parsia-Aref S. , Valizadegan O. , Farashiani M.E. (2015) Eucalyptus dundasii Maiden essential oil, chemical composition and insecticidal values against Rhyzopertha dominica (F.) and Oryzaephilus surinamensis (L.). , J. Plant Prot. Res., Vol.55 (1) ; pp.38-41
    31. Pimentel M.A. , Faroni L.R. , Batista M.D. , da Silva F.H. (2008) Resistance of stored-product insects to phosphine. , Pesqui. Agropecu. Bras., Vol.43 (12) ; pp.1671-1676
    32. Prakash A. , Rao J. (1997) Botanical pesticides in agriculture., CRC Press,
    33. Rafiei Karahroodi Z. , Moharramipour S. , Farazmand H. , Karimzadeh-Esfahani J. (2009) Effect of eighteen plant essential oils on nutritional indices of larvae Plodia interpunctella Hubner (Lep., Pyralidae). , J. Entomol. Res., Vol.1 (3) ; pp.209-219
    34. Rees D.P. (2007) Insects of stored grain: a pocket reference., Csiro Publishing,
    35. Regnault-Roger C. , Vincent C. , Arnason J.T. (2012) Essential oils in insect control: low-risk products in a high-stakes world. , Annu. Rev. Entomol., Vol.57 ; pp.405-424
    36. Rozman V. , Kalinovic I. , Korunic Z. (2007) Toxicity of naturally occurring compounds of Lamiaceae and Lauraceae to three storedproduct insects. , J. Stored Prod. Res., Vol.43 ; pp.349-355
    37. Saeidnia S. , Gohari A.R. , Mokhber-Dezfuli N. , Kiuchi F. (2011) A review on phytochemistry and medicinal properties of the genus Achillea. , Daru, Vol.19 ; pp.173-186
    38. Yang K. , Zhou Y.X. , Wang C.F. , Du S.S. , Deng Z.W. , Liu Q.Z. , Liu Z.L. (2011) Toxicity of Rhododendron anthopogonoidesessential oil and its constituent compounds towards Sitophilus zeamais. , Molecules, Vol.16 ; pp.7320-7330
    39. Zandi-Sohani N. , Ramezani L. (2015) Evaluation of five essential oils as botanical acaricides against the strawberry spider miteTetranychus turkestani Ugarov and Nikolskii. , Int. Biodeterior. Biodegradation, Vol.98 ; pp.101-106