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.

Results

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).

Discussion

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.