Abstract
The natural and ecologically safe control of stored product insects has gained considerable attention in modern society. In this study of further searching for botanical pesticides from wild-growing plant, the contact toxicity and repellency towards Tribolium castaneum and Liposcelis bostrychophila were assessed for the essential oil (EO) from Ostericum viridiflorum. The EO was distilled from aboveground parts of O. viridiflorum and checked by gas chromatography-mass spectrometry. Twenty-two compounds were identified and the main components were β-caryophyllene (24.3%), α-humulene (21.0%), apiol (10.2%), and carotol (2.5%). For bioactivity tests, results indicated that the EO and its two main compounds (β-caryophyllene and α-humulene) all showed potent contact toxicity towards L. bostrychophila with LD50 values of 44.52 μg/cm2, 74.11 μg/cm2, and 118.56 μg/cm2, respectively. The EO and the two main compounds also exhibited comparable repellency towards T. castaneum and L. bostrychophila. The results evidenced the EO of O. viridiflorum aboveground parts and its major compounds could be considered for the development of eco-friendly botanical insecticides and repellents in controlling stored product insects.
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Introduction
Pest infestation in stored products has been a major problem throughout the world. Pest insects cause substantial quantitative and qualitative losses of stored products (Karaborklu 2014). The red flour beetle, Tribolium castaneum, and the psocid, Liposcelis bostrychophila, are common and destructive stored product insects. Presently, the synthetic pesticides are widely used to control these insects. However, the widespread use of synthetic toxic pesticides has posed numerous problems including environmental pollution, possible health hazards to humans and animals, and the development of insecticide resistance due to their long persistence and accumulation in the environment and ecosystems (Tang et al. 2018; Bolognesi and Merlo 2011). Therefore, it is necessary to develop safe, eco-friendly, efficient pest control methods. In recent years, botanical pesticides, such as plant essential oil (EOs), are becoming increasingly popular as agents for control of a number of insect pests (Mukandiwa et al. 2016), vectors (Rajeswary et al. 2018), mites (Song et al. 2016), and ticks (Benelli and Pavela 2018). This is mainly attributed to EOs having multiple mechanisms of action, such as growth, development and fecundity reduction, molting and respiration disruption, acetylcholinesterase inhibition, and neurotoxic effects (Morya et al. 2010; Attia et al. 2012; Banken and Stark 1997; Dohi et al. 2009; Jankowska et al. 2018). EOs consist of diverse secondary metabolites that are biosynthesized by plants for specific functions, using different metabolic routes in plants. These secondary plant metabolites are complex mixtures of volatile molecules of low molecular weight, mainly terpenoids (monoterpenes and sesquiterpenes) and phenylpropanoids. The EOs generally are obtained by hydrodistillation, steam distillation, dry distillation, supercritical fluid extraction, and microwave-assisted process methods (Aziz et al. 2018). EOs have the advantage of low mammalian toxicity, rapid biodegradation with broad-spectrum activity, short environmental persistence, and minimal residual activity (Regnault-Roger et al. 2012). Many studies have demonstrated that EOs offer protection against insect pests through various activities, including contact and fumigant toxicities, larvicidal, ovicidal, adulticidal, and repellent activities, antifeedant, and oviposition deterrence effects (Sowndhararajan et al. 2017; Soonwera et al. 2018; Darabi and Khajehali 2017; Zahran et al. 2017). In addition to the bioactivities of EOs, there are some considerations and challenges for EOs (e.g., low stability and short persistence) that need to be solved (Pavela and Benelli 2016). During our ongoing search for new insecticides of plant origin, we have reported insecticidal activities of the EOs from two species (Ostericum sieboldii and O. grosseserratum) of genus Ostericum (Liu et al. 2011; Chu et al. 2013). In order to further search for botanical pesticides from genus Ostericum, this study continues to evaluate the bioactivities of EO from other species of this genus.
Ostericum (Family: Umbelliferae) is a separate subgenus from the genus Angelica on the basis of new phytochemical and molecular data, together with the serological data of Ostericum (Harborne et al. 1986; Shneyer et al. 2003; Suk et al. 1974). This genus comprises ten species distributed in North Korea, Japan, and the Far East, of which seven species are present in China (Pan et al. 1997). Among them, Ostericum viridiflorum (Turcz.) Kitagawa is a perennial herb with a yellowish brown conic root, purplish green and acute-angled stem, acute-triangular petioles, and triangular-ovate leaf blade. The inflorescence of compound umbel is 4–9 cm in diameter. Petals are green or greenish white. It is mainly distributed in northeast China and Inner Mongolia, and there are also distributions in eastern Siberia and the Far East. It grows in damp meadows, riversides, and stream banks (Gorovoi 1966; Kitagawa 1979; Fu and Hong 2001; Ohwi 1965; Park 2007). This plant is rich in valuable EOs, and has the ability of expelling wind, removing dampness, dispersing cold, and relieving pain. The young leaves of this plant are eaten as a spring vegetable and the roots are used to treat diseases like rheumatic pain, waist and knee pain, cold headache, and carbuncle swollen (Editorial Board of Zhong Hua Ben Cao, State Administration of Traditional Chinese Medicine 2004). Hence, in this study, we assess the contact toxicity and repellency of the EO from O. viridiflorum aboveground parts towards the red flour beetles and psocids for the first time. The first section of this paper analyzed the chemical composition of the EO from O. viridiflorum aboveground parts and then evaluated the contact toxicity and repellency towards the two stored product insects for the EO and its two major sesquiterpenes (α-humulene and β-caryophyllene).
Materials and methods
Essential oil extraction
Aboveground parts of O. viridiflorum were collected from Qianshan Mountain Scenic Spot, Anshan City, Liaoning Province, China (41.07° N latitude and 122.97° E longitude), in September 2016. The plant specimen was identified and authenticated by Prof. B. Fan from the Experimental Research Center, China Academy of Chinese Medical Sciences. The specimen (no. ERC-20160917) was deposited in the Herbarium (ERC) of Experimental Research Center. The sample was shade-dried at room temperature and grounded to powders. The ground powders were extracted by steam distillation for 8 h. The obtained EO sample was kept in hermetic brown bottle at 4 °C for further analysis.
Analysis of essential oil
GC-MS detection of the EO was conducted on Agilent 7890A GC-FID and Agilent 7890A GC-5975C MSD. The two systems were performed using the same condition. Analytical conditions were as follows: capillary column used HP-5MS (30 m × 0.25 mm × 0.25 μm) and temperature was set initially at 50 °C, kept for 1 min, and increased to 150 °C at 2 °C/min for 2 min, finally ramped to 240 °C at 10 °C/min. The injector was programmed at 250 °C. Dry helium was the carrier gas (1.0 mL/min). Volume of injected was 1 μL. Mass range was m/z 50 to 550. Identification of constituents was carried out by retention indices, compared to reported compounds in the literatures and authentic chemicals standards in authors’ laboratory. Under the same experimental conditions, the retention index for each compound was calculated with a standard n-alkanes series (C5–C36). Composition quantification was carried out using area normalization of the FID chromatograms.
Insect rearing
All tested insects used for the study were obtained from our laboratory cultures (Faculty of Geographical Science, Beijing Normal University) and were maintained for the last 2 years. The rearing was conducted under the dark in incubators at temperature of 28 to 30 °C and 60 to 70% r.h. Tribolium castaneum was fed on wheat flour mixed with yeast (10:1, w/w). The psocid was fed on an artificial diet composed of skim milk, dried yeast, as well as wholemeal (the proportion was 1:1:10). Adult unsexed beetles/booklice (1–2 weeks old) were employed in the further studies. All the insect containers and petri dishes were coated with polytetrafluoroethylene so that insects could not escape.
Contact toxicity
The contact toxicity towards T. castaneum for the EO and major constituents referenced the topical application method (Liu and Ho 1999). Range-finding studies were run to determine the appropriate testing concentrations. The EO and the two compounds were dissolved in n-hexane to obtain five series concentrations using serial dilution method. A volume of 0.5 μL of each dilution was dropped on the dorsal thorax of each insect. Both treatments and controls (using n-hexane) were put into glass bottles and then placed in incubators. The control and each test concentration were repeated five times with ten adult insects in each replication. Mortalities were recorded after 24 h. The bioassay of psocids was measured as residual film method (Zhao et al. 2012). n-Hexane was used to dilute five different concentrations of EO and compounds. A filter paper (5.5 cm diameter) was impregnated with 300 μL dilutions of each sample. Then the filter paper was posted in a Petri dish. Ten psocids were put in a Petri dish placed in an incubator and were exposed for 24 h after the lids were closed. Control group (using n-hexane) and each dose group were repeated five times.
Repellency tests
Repellency towards the red flour beetles for the EO and major constituents was measured following the method of Zhang et al. (2011). Five concentrations (0.13–78.63 nL/cm2) for each sample were designed together with the positive control DEET using n-hexane as solvent. Each treatment had a glass Petri dish (9 cm diameter) covered with the same size filter paper. This filter paper was split into two pieces, one half was added with 0.5 mL of each solution and the rest was considered as the control (0.5 mL of n-hexane). Both the two pieces were naturally dried leaving the residual n-hexane on them. As for psocids, the method used was similar to that described above and the only differences were the diameter of Petri dishes and filter papers (5.5 cm), five series concentration for each sample (0.10–63.17 nL/cm2), and the treatment dose (150 μL). Twenty beetles/booklice were located in the middle of filter paper for each assay, and the Petri dishes were transferred to incubators after the lids of Petri dish were closed. The experiment in each group was repeated five times and the percent repellency (PR) of each sample was counted at 2 and 4 h as follows: PR (%) = [(Nc-Nt)/(Nc + Nt)] × 100, N = number of insects; c = negative control half; t = treated half.
Data analysis
The mortality data generated in contact toxicity assay were calculated by Abbott’s formula to obtain natural mortality (Fleming and Retnakaran 1985). The LD50 values, their 95% confidence intervals, slope, and chi-square values were estimated by Probit analysis. In repellency tests, the percentages were normalized using square arcsine transformation before ANOVA. Mean (±SE) values were compared and differed using Tukey’s test (SPSS version 19.0, Windows XP) (Jia 2006).
Results and discussion
Chemical constituents of essential oil
The aboveground parts of O. viridiflorum yielded 0.025% EO. Totally, 22 compounds, accounting for 70.2% of the EO of O. viridiflorum aboveground parts, were detected (Table 1). The main constituents of EO from O. viridiflorum aboveground parts were β-caryophyllene (24.3%), α-humulene (21.0%), apiol (10.2%), and carotol (2.5%). The results were not in accordance with the only one published report on the components of the EO of O. viridiflorum aboveground parts from Shkotovo, Shkotovskii District; the major compounds of the EO were caryophyllene oxide (61.7%), 3,4-dimethyl-3-cyclohexan-1-carboxaldehdye (5.8%), isobutyl-2-methylpent-3-yl ester of phthalic acid (5.5%), and vulgarol (4.0%) (Suleimen et al. 2014). Though there was only one report on the constituents of the EO of O. viridiflorum, there were a few reports on the components of EOs from other species of Ostericum. For example, Song et al. (2015) found that β-phellandrene (38.2%), α-bisabolol (9.4%), m-cresol (6.7%), terpinolen (5.5%), and 1-acetoxy-1,2-epoxycyclohexane (5.0%) were the principal constituents of the EO of O.koreanum rhizome collected from Jeonju, Korea. Moreover, α-pinene (41.1%), ρ-cresol (18.0%), 4-methylacetophenone (7.9%), sabinene (7.6%), and α-bisabolol (2.1%) were detected in the EO of O. koreanum leaves from Chungcheongbuk-do, Jecheon, South Korea (Shin 2005). The differences in EO composition and content from the same species might be arise from various external or internal factors such as the geographical location, collection parts, harvest time, climate, storage duration, as well as plant parts (roots, leaves, flowers, and stems), which may affect different biological activities (Salamon 2007). Therefore, further studies regarding EO quality control and standardization are required.
Contact toxicity
The EO showed potent contact toxicity towards psocids as it exhibited a LD50 value of 44.52 μg/cm2, but displayed weak toxicity against T. castaneum within measurement range (Table 2). The EO possessed only 2.4 times less toxicity than pyrethrins (positive control, LD50 = 18.72 μg/cm2) against psocids. Meanwhile, the EO showed higher contact toxicity against psocids than the two main compounds, which had almost 2.7 and 1.7 times more toxicity than α-humulene (LD50 = 118.56 μg/cm2) and β-caryophyllene (LD50 = 74.11 μg/cm2) against psocids. The high toxicity of the EO against psocids could be due to the interaction between major compounds and others. The other ingredients in the oil often play a key part in contact toxicity. Such as β-caryophyllene oxide (1.5%), it exhibited strong contact toxicity against psocids with LD50 values of 35.40 μg/cm2 and 27.20 μg/cm2 respectively in the previous reports (Cao et al. 2018a, b). From the above, β-caryophyllene oxide and structural analogues (α-humulene and β-caryophyllene) all demonstrated potent contact toxicity against psocids. By comparing the chemical structures with their bioactivity, these three sesquiterpenes had the same sesquiterpene structure (an 11-membered macrocycle). However, as for the red flour beetles, α-humulene (LD50 = 14.23 μg/cm2), β-caryophyllene (LD50 = 41.72 μg/cm2), and β-caryophyllene oxide (LD50 = 45.56 μg/cm2) (Liu et al. 2012) exhibited less toxicity (no overlap in 95% fiducial limit) than the positive control, pyrethrins (LD50 = 0.26 μg/cm2), suggesting that the sesquiterpene structure may have more effective toxic properties against the psocids than against the red flour beetles. It should be added that further research is needed to explore the insecticidal mechanism of above sesquiterpene hydrocarbons.
Repellent activity
The repellent effect produced by the EO and its major sesquiterpenes towards red flour beetles and psocids was observed in Tables 3 and 4. It was found that this EO demonstrated high repellency against both T. castaneum and L. bostrychophila, especially towards T. castaneum. The EO and DEET exhibited the same level of repellent activity against red flour beetles at high concentrations (78.63 and 15.73 nL/cm2) after 2- and 4-h treatment. Moreover, at low concentrations, EO even exhibited higher repellency than DEET against red flour beetles. For example, at three low concentrations (3.15, 0.63, and 0.13 nL/cm2), EO (80, 72, and 52%, respectively) exhibited significantly stronger repellency than DEET (68, 54, and 22%, respectively) against T. castaneum at 4 h. Unlike the repellency on T. castaneum, data in Table 4 explained that the EO had high repellency against psocids only at the high concentrations (≥ 12.63 nL/cm2). At high concentrations (63.17 and 12.63 nL/cm2), compared with DEET, the EO showed higher repellency against psocids after 2- and 4-h treatment. Especially at the highest dose (63.17 nL/cm2), the EO both showed 100% repellency against psocids at 2 and 4 h when compared with DEET (94% and 92%). The repellency of the EO tended to reduce with decreasing concentration of sample. At the lowest concentration (0.10 nL/cm2), compared with DEET (56% and 28%), the EO (10% and 8%) showed weaker repellency against psocids at 2 and 4 h after exposure. The two main compounds α-humulene and β-caryophyllene showed different levels of repellency against the two insects. As for T. castaneum, at testing doses of 78.63, 15.73, and 3.15 nL/cm2, α-humulene demonstrated stronger repellent activity than β-caryophyllene at 2 and 4 h, while β-caryophyllene showed stronger repellent activity than α-humulene at testing doses of 0.63 and 0.13 nL/cm2 at both 2 and 4 h. Further, at the dose of 0.13 nL/cm2, β-caryophyllene (22%) showed much stronger repellency at 2 h relative to DEET (8%). However, as for L. bostrychophila, at five tested concentrations, β-caryophyllene exhibited higher repellency than α-humulene at both 2 and 4 h, except for the concentration of 0.10 nL/cm2 at 4 h. Furthermore, at testing dose of 63.17 and 12.63 nL/cm2, the PR of β-caryophyllene both reached 100% at 2 h when compared with DEET (94% and 82%), suggesting that β-caryophyllene was strongly repellent towards L. bostrychophila. The repellent activity of α-humulene and β-caryophyllene has also been observed towards other insects. For example, previous research in the literature reported that α-humulene and β-caryophyllene both showed strong repellency on Ixodes ricinus (Ashitani et al. 2015). Moreover, α-humulene and β-caryophyllene achieved various degrees of repellency against Tetranychus urticae (Araújo et al. 2012). However, as for Aedes aegypti, α-humulene showed weak repellency, β-caryophyllene was not active repellent even at the maximum test dose (Zhai et al. 2017).
α-Humulene and β-caryophyllene were similar in chemical structure and were often found together as a mixture in many aromatic plants, but their bioactivities were different in this study. It is interesting to note that α-humulene possessed higher contact toxicity than β-caryophyllene against T. castaneum; however, α-humulene had less toxicity than β-caryophyllene against booklice. In repellency assay, β-caryophyllene demonstrated higher repellency than α-humulene against red flour beetles only at the low concentrations (0.63 and 0.13 nL/cm2), while β-caryophyllene possessed comparatively higher repellency than α-humulene against booklice almost at five tested concentrations. α-Humulene is a natural cyclic sesquiterpene with an 11-membered ring containing three isoprene units (Neuenschwander et al. 2012). β-Caryophyllene is an isomer of humulene and has a humulene macrocycle structure with a bicyclic 4/9 ring system, in which a trans double bond in the nine-membered ring (Tanaka et al. 1996). The molecular structural differences of the two compounds and the mechanism of insect species may account for the significant difference in bioactivities.
On the other hand, α-humulene and β-caryophyllene were natural isomeric sesquiterpenes, widely existing in the EOs of many medicinal and spice plants. β-Caryophyllene has been shown to have various biological activities, such as antimicrobial, phage repellent, local anesthetic, anti-inflammatory, anti-tumoral, anti-allergic, as well useful as a flavoring agent (Tambe et al. 1996; Budavari et al. 1996; Sköld et al. 2006). Moreover, β-caryophyllene exhibited good activities against a wide range of insects, e.g., the larvae of mosquito vectors (Aedes albopictus, Anopheles subpictus, and Culex tritaeniorhynchus), Spodoptera frugiperda, T. castaneum, Lasioderma serricorne, and Cacopsylla chinensis (Govindarajan et al. 2016; Cárdenas-Ortega et al. 2015; Chaubey 2012; Pandey and Singh 2017; Tian et al. 2015). In addition, α-humulene was also associated with many bioactivities (such as anti-tumor, anti-fungal, anti-asthma, anti-allergies, anti-inflammatory, and inhibition of drug-metabolizing enzymes) and was often used as an inevitable ingredient during the brewing process (Legault et al. 2003; Sabulal et al. 2006; Rogerio et al. 2010; Passos et al. 2007; Nguyen et al. 2017; Connolly and Hill 1991). In recent studies, α-humulene was reported to have bioactivities in control of insects, e.g., L. serricorne, L. bostrychophila, larvae of A. subpictus, A. albopictus, and C. tritaeniorhynchus, and Helicoverpa armigera (Guo et al. 2017; Govindarajan and Benelli 2016; Benelli et al. 2018).
In conclusion, the above results indicated that the EO and its two main constituents would be the exploration direction of botanical insecticides and repellents in controlling stored product insects.
Conclusion
The present study analyzed the composition of the EO of O. viridiflorum aboveground parts and reported for the first time the toxicity and repellent activity of the EO against the two storage pests. The results of this study demonstrate that the EO and the two selected constituents could play a vital role in the integrated pest management of stored products and safeguard the environment and health of the user from the risk of the use of synthetic insecticides. Moreover, the EOs from three species (O. viridiflorum, O. sieboldii, and O. grosseserratum) of Ostericum all showed bioactivities against stored product insects in our series of studies. This work would not only provide a scientific foundation for further development and utilization of O. viridiflorum resource in control of stored product insects but also establish a very good perspective for comprehensive utilization of plant resources of Ostericum genus. However, there are also a number of challenges (such as stability, standardization of chemical composition, quality control, non-target toxicity, and micro-encapsulation of the most effective molecules) for EOs to face, which deserve further study and discussion.
References
Araújo MJC, Câmara CAG, Born FS, Moraes MM, Badji CA (2012) Acaricidal activity and repellency of essential oil from Piper aduncum and its components against Tetranychus urticae. Exp Appl Acarol 57(2):139–155
Ashitani T, Garboui SS, Schubert F, Vongsombath C, Liblikas I, Pålsson K, Borg-Karlson AK (2015) Activity studies of sesquiterpene oxides and sulfides from the plant Hyptis suaveolens (Lamiaceae) and its repellency on Ixodes ricinus (Acari: Ixodidae). Exp Appl Acarol 67(4):595–606
Attia S, Grissa KL, Mailleux AC, Heuskin S, Lognay G, Hance T (2012) Acaricidal activities of Santolina africana and Hertia cheirifolia essential oils against the two-spotted spider mite (Tetranychus urticae). Pest Manag Sci 68(7):1069–1076
Aziz ZAA, Ahmad A, Setapar SHM, Karakucuk A, Azim MM, Lokhat D, Rafatullah M, Ganash M, Kamal MA, Ashraf GM (2018) Essential oils: extraction techniques, pharmaceutical and therapeutic potential: a review. Curr Drug Metab 19(13). https://doi.org/10.2174/1389200219666180723144850
Banken JAO, Stark JD (1997) Stage and age influence on the susceptibility of Coccinella septempunctata (Coleoptera: Coccinellidae) after direct exposure to Neemex, a neem insecticide. J Econ Entomol 90(5):1102–1105
Benelli G, Pavela R (2018) Repellence of essential oils and selected compounds against ticks: a systematic review. Acta Trop 179:47–54
Benelli G, Govindarajan M, Rajeswary M, Vaseeharan B, Alyahya SA, Alharbi NS, Kadaikunnan S, Khaled JM, Maggi F (2018) Insecticidal activity of camphene, zerumbone and α-humulene from Cheilocostus speciosus rhizome essential oil against the Old-World bollworm, Helicoverpa armigera. Ecotox Environ Safe 148:781–786
Bolognesi C, Merlo FD (2011) Pesticides: human health effects. Encyclopedia Environ Health 156(1):438–453
Budavari S, O’neil MJ, Smith A, Heckelman PE, Kinneary JF (1996) The Merck index: an encyclopedia of chemicals, drugs, and biologicals, 12th edn. Merck and Co, Inc, Whitehouse Station
Cao JQ, Guo SS, Wang Y, Pang X, Geng ZF, Du SS (2018a) Contact toxicity and repellency of the essential oils of Evodia lenticellata Huang and Evodia rutaecarpa (Juss.) Benth. Leaves against three stored product insects. J Oleo Sci 67(8):1027–1034
Cao JQ, Guo SS, Wang Y, Pang X, Geng ZF, Du SS (2018b) Toxicity and repellency of essential oil from Evodia lenticellata Huang fruits and its major monoterpenes against three stored-product insects. Ecotox Environ Safe 160:342–348
Cárdenas-Ortega NC, González-Chávez MM, Figueroa-Brito R, Flores-Macías A, Romo-Asunción D, Martínez-González DE, Pérez-Moreno V, Ramos-López MA (2015) Composition of the essential oil of Salvia ballotiflora (Lamiaceae) and its insecticidal activity. Molecules 20(5):8048–8059
Chaubey MK (2012) Acute lethal and synergistic effects of some terpenes against Tribolium castaneum herbst (Coleoptera: Tenebrionidae). Ecol Balk 4(1):53–62
Chu SS, Liu QZ, Du SS, Liu ZL (2013) Chemical composition and insecticidal activity of the essential oil of the aerial parts of Ostericum grosseserratum (Maxim) Kitag (Umbelliferae). Trop J Pharm Res 12(1):99–103
Connolly JD, Hill RA (1991) Dictionary of terpenoids. Chapman and Hall, London
Darabi K, Khajehali J (2017) Bioactivity of essential oils of Mentha species and Cuminum cyminum L. on Anarta trifolii (Hufnagel) (Lepidoptera: Noctuidae). J Essent Oil Bear Plants 20(4):1097–1106
Dohi S, Terasaki M, Makino M (2009) Acetylcholinesterase inhibitory activity and chemical composition of commercial essential oils. J Agric Food Chem 57(10):4313–4318
Editorial Board of Zhong Hua Ben Cao, State Administration of Traditional Chinese Medicine (2004) Zhong Hua Ben Cao (Chinese herbal Medicine), Vol 32. Shanghai Science and Technology Press, Shanghai (in Chinese)
Fleming R, Retnakaran A (1985) Evaluating single treatment data using Abbott’s formula with reference to insecticides. J Econ Entomol 78(6):1179–1181
Fu LG, Hong T (2001) Higher plants of China, Vol 8. Qingdao Publishing House, Qingdao (in Chinese)
Gorovoi PG (1966) Umbelliferae of primorye and priamurye. Nauka, Leningrad (in Russian)
Govindarajan M, Benelli G (2016) α-Humulene and β-elemene from Syzygium zeylanicum (Myrtaceae) essential oil: highly effective and eco-friendly larvicides against Anopheles subpictus, Aedes albopictus, and Culex tritaeniorhynchus (Diptera: Culicidae). Parasitol Res 115(7):2771–2778
Govindarajan M, Rajeswary M, Hoti SL, Bhattacharyya A, Benelli G (2016) Eugenol, α-pinene and β-caryophyllene from Plectranthus barbatus essential oil as eco-friendly larvicides against malaria, dengue and Japanese encephalitis mosquito vectors. Parasitol Res 115(2):807–815
Guo SS, Zhang WJ, You CX, Liang JY, Yang K, Geng ZF, Du SS, Wang CF (2017) Chemical composition of essential oil extracted from Laggera pterodonta and its bioactivities against two stored product insects. J Food Process Preserv 41(2). https://doi.org/10.1111/jfpp.12941
Harborne JB, Heywood VH, Chen XY (1986) Separation of Ostericum from Angelica on the basis of leaf and mericarp flavonoids. Biochem Syst Ecol 14(1):81–83
Jankowska M, Rogalska J, Wyszkowska J, Stankiewicz M (2018) Molecular targets for components of essential oils in the insect nervous system: a review. Molecules 23(1). https://doi.org/10.3390/molecules23010034
Jia CS (2006) Calculating the LC50 of insecticides with software SPSS. Chin B Entomol 43(3):414–417
Karaborklu S (2014) Chemical characterization of Sideritis perfoliata L. essential oil and its fumigant toxicity against two pest insects. J Food Agric Environ 12(2):434–437
Kitagawa M (1979) Neo-lineamenta florae Manshuricae. J Cramer, Vaduz
Legault J, Dahl W, Debiton E, Pichette A, Madelmont JC (2003) Antitumor activity of balsam fir oil: production of reactive oxygen species induced by alpha-humulene as possible mechanism of action. Planta Med 69(5):402–407
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
Liu ZL, Chu SS, Jiang GH (2011) Insecticidal activity and composition of essential oil of Ostericum sieboldii (Apiaceae) against Sitophilus zeamais and Tribolium castaneum. Rec Nat Prod 5(2):74–81
Liu P, Liu XC, Dong HW, Liu ZL, Du SS, Deng ZW (2012) Chemical composition and insecticidal activity of the essential oil of Illicium pachyphyllum fruits against two grain storage insects. Molecules 17(12):14870–14881
Morya K, Pillai S, Patel P (2010) Effect of powdered leaves of Lantana camara, Clerodendrum inerme and Citrus limon on the rice moth Corcyra cephalonica. B Insectol 63(2):183–189
Mukandiwa L, Naidoo V, Katerere DR (2016) The use of Clausena anisata in insect pest control in Africa: a review. J Ethnopharmacol 194:1103–1111
Neuenschwander U, Czarniecki B, Hermans I (2012) Origin of regioselectivity in α-humulene functionalization. J Organomet Chem 77(6):2865–2869
Nguyen LT, Myslivečková Z, Szotáková B, Špičáková A, Lněničková K, Ambrož M, Kubíček V, Krasulová K, Anzenbacher P, Skálová L (2017) The inhibitory effects of β-caryophyllene, β-caryophyllene oxide and α-humulene on the activities of the main drug-metabolizing enzymes in rat and human liver in vitro. Chem Biol Interact 278:123–128
Ohwi J (1965) Flora of Japan. Smithsonian Institution, Washington
Pan ZH, Liu XT, Li XH, Yao XM, Zhuang TD, Lin X (1997) A study on karyotypes and geographical distribution of Ostericum (Umbelliferae) in China. Acta Phytotaxon Sin 35(6):511–520
Pandey AK, Singh P (2017) The genus Artemisia: a 2012-2017 literature review on chemical composition, antimicrobial, insecticidal and antioxidant activities of essential oils. Medicines 4(3). https://doi.org/10.3390/medicines4030068
Park CW (2007) The genera of vascular plants of Korea. Flora of Korea Editorial Committee, Seoul
Passos GF, Fernandes ES, da Cunha FM, Ferreira J, Pianowski LF, Campos MM, Calixto JB (2007) Anti-inflammatory and anti-allergic properties of the essential oil and active compounds from Cordia verbenacea. J Ethnopharmacol 110(2):323–333
Pavela R, Benelli G (2016) Essential oils as ecofriendly biopesticides? Challenges and constraints. Trends Plant Sci 21(12):1000–1007
Rajeswary M, Govindarajan M, Alharbi NS, Kadaikunnan S, Khaled JM, Benelli G (2018) Zingiber cernuum (Zingiberaceae) essential oil as effective larvicide and oviposition deterrent on six mosquito vectors, with little non-target toxicity on four aquatic mosquito predators. Environ Sci Pollut Res Int 25(11):10307–10316
Regnault-Roger C, Vincent C, Arnason JT (2012) Essential oils in insect control: low-risk products in a high-stakes world. Annu Rev Entomol 57:405–424
Rogerio AP, Andrade EL, Leite DFP, Figueiredo CP, Calixto JB (2010) Preventive and therapeutic anti-inflammatory properties of the sesquiterpene α-humulene in experimental airways allergic inflammation. Br J Pharmacol 158(4):1074–1087
Sabulal B, Dan M, AJ J, Kurup R, Pradeep NS, Valsamma RK, George V (2006) Caryophyllene-rich rizhome oil of Zingiber mimmonii from South India: chemical characterization and antimicrobial activity. Phytochemistry 67(22):2469–2473
Salamon I (2007) Effect of the internal and external factors on yield and qualitative-quantitative characteristics of chamomile essential oil. Acta Hortic 749:45–64
Shin S (2005) In vitro effects of essential oils from Ostericum koreanum against antibiotic-resistant Salmonella spp. Arch Pharm Res 28(7):765–769
Shneyer VS, Kutyavina NG, Pimenov MG (2003) Systematic relationships within and between Peucedanum and Angelica (Umbelliferae-Peucedaneae) inferred from immunological studies of seed proteins. Plant Syst Evol 236(3–4):175–194
Sköld M, Karlberg AT, Matura M, Börje A (2006) The fragrance chemical β-caryophyllene-air oxidation and skin sensitization. Food Chem Toxicol 44(4):538–545
Song JE, Yang JY, Lee HS (2015) Comparison with volatile compounds derived from essential oils of Ostericum spp. roots in Korea. J Essent Oil Bear Pl 18(6):1417–1420
Song JE, Kim JM, Lee NH, Yang JY, Lee HS (2016) Acaricidal and insecticidal activities of essential oils against a stored-food mite and stored-grain insects. J Food Prot 79(1):174–178
Soonwera M, Wongnet O, Sittichok S (2018) Ovicidal effect of essential oils from Zingiberaceae plants and Eucalytus globulus on eggs of head lice, Pediculus humanus capitis De Geer. Phytomedicine 47:93–104
Sowndhararajan K, Deepa P, Kim M, Park SJ, Kim S (2017) A review of the composition of the essential oils and biological activities of Angelica Species. Sci Pharm 85(3):33. https://doi.org/10.3390/scipharm85030033
Suk KT, Nitta A, Konoshima M (1974) Studies on origin of Japanese Chuanxiong II. Ostericum. Yakugaku Zasshi 94(10):1246–1250
Suleimen EM, Iskakova ZB, Dudkin RV, Gorovoi PG, Wang M, Khan I, Ross SA, Martins CHG (2014) Composition and biological activity of essential oils from east-asian species Angelica viridiflora, A. cincta, and Coelopleurum gmelinii. Chem Nat Compd 50(6):1136–1139
Tambe Y, Tsujiuchi H, Honda G, Ikeshiro Y, Tanaka S (1996) Gastric cytoprotection of the non-steroidal anti-inflammatory sesquiterpene, beta-caryophyllene. Planta Med 62(5):469–470
Tanaka S, Akimoto M, Tambe Y, Tabata M, Ikeshiro Y (1996) Volatile antiallergic principles from a traditional herbal prescription of Kampo medicine. Phytother Res 10(3):238–241
Tang WX, Wang D, Wang JQ, Wu ZW, Li LY, Huang ML, Xu SH, Yan DY (2018) Pyrethroid pesticide residues in the global environment: an overview. Chemosphere 191:990–1007
Tian BL, Liu QZ, Liu ZL, Li P, Wang JW (2015) Insecticidal potential of clove essential oil and its constituents on Cacopsylla chinensis (Hemiptera: Psyllidae) in laboratory and field. J Econ Entomol 108(3):957–961
Yang K, Wang CF, You CX, Geng ZF, Sun RQ, Guo SS, Du SS, Liu ZL, Deng ZW (2014) Bioactivity of essential oil of Litsea cubeba from China and its main compounds against two stored product insects. J Asia Pac Entomol 17(3):459–466
You CX, Yang K, Wu Y, Zhang WJ, Wang Y, Geng ZF, Chen HP, Jiang HY, Du SS, Deng ZW (2014) Chemical composition and insecticidal activities of the essential oil of Perilla frutescens (L.) Britt aerial parts against two stored product insects. Eur Food Res Technol 239(3):481–490
Zahran HEM, Abou-Taleb HK, Abdelgaleil SAM (2017) Adulticidal, larvicidal and biochemical properties of essential oils against Culex pipiens L. J Asia Pac Entomol 20(1):133–139
Zhai CM, Wang M, Raman V, Rehman JU, Meng YH, Zhao JP, Avula B, Wang YH, Tian ZK, Khan IA (2017) Eleutherococcus senticosus (Araliaceae) leaf morpho-anatomy, essential oil composition, and its biological activity against Aedes aegypti (Diptera: Culicidae). J Med Entomol 54(3):658–669
Zhang JS, Zhao NN, Liu QZ, Liu ZL, Du SS, Zhou L, Deng ZW (2011) Repellent constituents of essential oil of Cymbopogon distans aerial parts against two stored-product insects. J Agric Food Chem 59(18):9910–9915
Zhao NN, Zhou LG, Liu ZL, Du SS, Deng ZW (2012) Evaluation of the toxicity of the essential oils of some common Chinese spices against Liposcelis bostrychophila. Food Control 26(2):486–490
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Zhang, H.M., Guo, S.S., Fan, B. et al. Evaluation of efficacy of the essential oil from Ostericum viridiflorum (Turcz.) Kitagawa in control of stored product insects. Environ Sci Pollut Res 26, 1406–1413 (2019). https://doi.org/10.1007/s11356-018-3728-x
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DOI: https://doi.org/10.1007/s11356-018-3728-x