Abstract
The essential oils (EOs) from aerial parts of Saussurea amara (L.) DC. (SAEO) and Sigesbeckia pubescens Makino (SPEO) were analyzed for their chemical composition by GC-MS, and their repellent activities against adults of the red flour beetle, Tribolium castaneum Herbst, as well as the booklouse, Liposcelis bostrychophila Badonnel, were evaluated for the first time. Results of GC-MS analysis indicated that both SAEO and SPEO were characterized by high content of sesquiterpenoids (relative content > 70%) including oxygenated sesquiterpenoids. The two oil samples and their major component caryophyllene oxide exerted beneficial repellent effects on T. castaneum and L. bostrychophila at 2 and 4 h post-exposure. At 4 h post-exposure, the PR value of caryophyllene oxide could still reach 92% (class V) against T. castaneum at minimum testing concentration of 3.15 nL/cm2, and this compound was observed to result in the greatest repellency (PR = 100%) against L. bostrychophila at 12.63 nL/cm2. This work confirmed the potent repellent efficacy of SAEO and SPEO for controlling pest damage and suggested their potential to be developed into botanical repellents.
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Introduction
Over the years, synthetic pesticides and repellents were widely applied in pest management. Extensive use of commercially available chemicals has led to developing resistance in a variety of pest species, and negative effects on humans and environment (Jun-Hyung et al. 2016; Spochacz et al. 2018). Essential oils (EOs) derived from plants have drawn more attention owing to their expected advantages, such as easier biodegradability in the environment and wide bioactivities (Jun-Hyung et al. 2017; Asgar and Sendi 2015). The number of articles in this field published annually with amazing growth (Isman and Grieneisen 2014). EOs that serve as by-products of plant metabolism are usually composed of several major components at fairly high concentrations and minor constituents present in trace amounts (Jun-Hyung et al. 2016). Major components tend to determine biological effects that EOs display (Pavela 2015).
Repellency represents one of common ways in pest management (De Oliveira et al. 2018). A repellent can cause target insects to make a directed movement away from a treated surface following contact or vapor-phase exposure. N,N-diethyl-3-methylbenzamide (DEET) is a broad-spectrum synthetic repellent with good activity against various insects. However, overuse and abuse of this commercial chemical has triggered its degraded efficacy and disrupted natural ecosystems to some degree. Besides, DEET was reported to correlate with some toxic reactions in humans including seizures and encephalopathy in children (Tabanca et al. 2016). Botanical repellents based on EOs are generally investigated due to their diverse chemical composition, high effectiveness against a wide range of pests, and low toxicity against non-target organisms including humans (Pavela and Benelli 2016). Even so, it inevitably has certain flaws. Active compounds in EOs are always rapidly volatilized (López and Pascual-Villalobos 2015), and meanwhile their specificity towards targeted pests is not as high as that of their synthetic counterparts (De Oliveira et al. 2014). Currently, nanobiotechnology offers a great promise to improve the stability and effectiveness of these natural products. Nanotechnological formulations could help botanical products rigorously standardized to an extent thus to ensure a certain level of potency in the practical application (De Oliveira et al. 2014, 2018).
Essential oils extracted from many Compositae plants were found to have remarkable bioactivities against stored-product insects (Guo et al. 2019). Saussurea amara (L.) DC. (Saussurea) and Sigesbeckia pubescens Makino (Sigesbeckia) are two species of the family Compositae. They have been used as traditional medicinal herbs in China since centuries ago (Avdeeva et al. 2017; Gao et al. 2018). As previously reported, some Saussurea plants had insecticidal, repellent, or growth-inhibiting activities against mosquito vectors and storage pests especially from Coleoptera. The essential oil from aerial parts of Sa. nivea Turcz. had strong contact and fumigant toxicity against Sitophilus zeamais Motsch (Chu et al. 2012). Acetone extracts of Sa. lappa Clarke were the effective repellents and growth inhibitor against T. castaneum (Kanvil et al. 2006; Chander et al. 1999), and the root oil of this plant with large amounts of sesquiterpenoids exhibited larvicidal activity against Aedes albopictus Skuse (Liu et al. 2012a, 2012b). Methanol extracts of Sa. heteromala (D.Don) showed certain toxicity to the jute hairy caterpillar, Spilosoma obliqua Walker (Lep.: Erebidae) (Gautam and Rao 2003). Moreover, anti-insect properties of Sigesbeckia plants have been rarely reported so far. Only Si. orientalis L. retrieved few published articles. The EO of its twigs exhibited repellency against Callosobruchus chinensis (L.) and C. maculatus (Col.: Chrysomelidae) (Pandey et al. 2013), and ethanol extracts of its leaves showed significant antifeedant activities against the cabbage webworm Crocidolomia binotalis Zeller (Lep.: Pyralidae) (Facknath and Kawol 1993). The two Compositae species Sa. amara and Si. pubescens have not been evaluated for pest control.
The red flour beetle, Tribolium castaneum Herbst (Col.: Tenebrionidae), and the booklouse, Liposcelis bostrychophila Badonnel (Psocoptera: Liposcelididae), common insects in warehouses and grain stores, could result in irretrievable damage to stored crops, grains, and the like (Abdullahi et al. 2018; Howard and Lord 2003). In this work, the two kinds of storage pests were selected as targeted insects to assess repellent activities of EOs from Sa. amara (SAEO) and Si. pubescens (SPEO). This work provides some scientific evidences and ideas for the development of botanical repellents and comprehensive utilization of plant resources.
Materials and methods
Plant materials and essential oil extraction
The aerial parts of Saussurea amara and Sigesbeckia pubescens were collected from Qianshan, Liaoning Province, China, in September 2013. Plant samples were identified by Dr. Q. R., Liu. (College of Life Sciences, Beijing Normal University, Beijing, China). Voucher specimens (labelled as BNU-CMH-Dushushan-2013-09-22-01 and BNU-CMH-Dushushan-2013-09-21-01, respectively) were deposited in the Herbarium of the College of Resources Science and Technology, Faculty of Geographical Science, Beijing Normal University. Two authentic plant materials were separately air-dried under room conditions and subjected to hydrodistillation using a modified Clevenger-type apparatus for 6 h. The volumes of essential oils obtained were recorded by observing the graduated part of Clevenger-type apparatus for yield calculation. Then, the oil samples were dried over anhydrous sodium sulfate and stored in an airtight container at 4 °C for further investigation.
Chemicals
C8-C24n-alkanes were purchased from Sigma-Aldrich (St. Louis, MO, USA). N,N-diethyl-3-methylbenzamide (DEET) was purchased from the National Center of Pesticide Standards (Shenyang, China). (E)-caryophyllene (95%) and caryophyllene oxide (95%) were purchased from Acros Organics (NewJersey, USA). Acetone (A.R.) was purchased from Beijing Chemical Works (Beijing, China).
Target insects
Tribolium castaneum and Liposcelis bostrychophila were obtained from laboratory cultures, which were kept in dark incubators at 28–30 °C and 70–80% relative humidity. T. castaneum was reared at a mixture of wheat flour and active yeast (ratio: 10/1, w/w). L. bostrychophila was fed on a mixture of wheat flour, milk powder, and active yeast (ratio 10/1/1, w/w/w). The unsexed adults about 1–2 weeks old were adopted for the following bioassays.
GC-FID and GC-MS analysis
GC-MS analysis was carried out on a Thermo Finnigan Trace DSQ instrument (Thermo Finnigan, Lutz, FL, USA) with a capillary column of HP-5MS (30 m × 0.25 mm × 0.25 μm). It was operated under the following conditions: injector temperature 250 °C, oven temperature programmed 50–250 °C (50–150 °C at 2 °C/min; 150–250 °C at 10 °C/min), carrier gas helium (1 mL/min), injected volume 1 μL (1% solution, v/v), split ratio 1:20. Spectra were scanned from 50 to 550 m/z. Identification of the oil constituents was dependent on the comparison of retention index (RI) and mass spectra with those recorded in Adams and the NIST05 library (Adams 2001). RI values were calculated based on the retention time of a homologous series of n-alkanes (C8-C24). Quantification analysis used the gas chromatograph (Thermo Finnigan Trace DSQ) equipped with a flame ionization detector (FID). Relative percentages of individual components in the EOs were obtained from GC-FID analysis reports by peak area integration, without application of correction factors.
Repellent assay
The evaluation of repellent activity followed the methods of Wang et al. (2019). Acetone was used as the negative control and DEET (N, N-diethyl-3-methyl-benzamide) as the positive control. For T. castaneum, the testing solutions of EOs/compounds with three concentrations (78.63, 15.73, 3.15 nL/cm2) were prepared in acetone. The filter paper (9 cm in diameter) was cut in half, and 500 μL of testing solutions was applied separately to a half-filter paper with a micropipette, as uniformly as possible. The other half was treated with an equal volume of acetone. Then, the two halves were air-dried to evaporate the solvent and stuck together on a Petri dish, which was used to confine insects here. In terms of booklice, the Petri dishes and filter papers were 5.5 cm in diameter and the concentrations of EOs/compounds were set at 63.17, 12.63, and 2.53 nL/cm2. Two halves of a filter paper were treated with 150 μL of the testing solutions. In all bioassays, 20 insects were released in the center of each filter paper disk and a cover was placed over the dish. Five replicates were carried out for each concentration. The number of insects present on the treated and control portions of each filter paper was recorded at 2 and 4 h post-exposure.
Data analysis
In the repellent assays, the percent repellency (PR) was determined by the following equation (Wang et al. 2019): PR (%) = [(Nc − Nt)/(Nc + Nt)] × 100. Here, Nc = the number of insects on the control half and Nt = the number of insects on the treated half. Percentage repellency values were transformed into arcsine and square root values for data standardization before one-way ANOVA (Tukey’s HSD test). Differences between means were considered statistically significant when “P < 0.05.” Meanwhile, the mean PR values were assigned to several classes (0 to V), repellency %: 0, > 0.01 to < 0.1; I, 0.1–20.0; II, 20.1–40.0; III, 40.1–60.0; IV, 60.1–80.0; and V, 80.1–100 (Liu and Ho 1999).
Results and discussion
Chemical composition of the essential oils
The yields of SAEO and SPEO were approximately 0.02% and 0.01% (v/w, mL/g), which were not considerable for extraction here. Hydrodistillation in the modified Clevenger system is frequently applied in the laboratory preparation of EOs. An effective method is essential for increasing the oil yield. Thus the optimization of extractive conditions becomes a crucial practice in the experimental investigation. It is significant to raise yield and meanwhile keep consistent outcomes of the oil composition, which can help ponder a scalable use in industrial settings (Sadeh et al. 2019). Results of GC-MS analysis are shown in Table 1. SAEO and SPEO had large amounts of sesquiterpenoids (71.2% and 74.0% respectively). In SPEO, oxygenated sesquiterpenoids represented 62.5% of the oil composition. The most abundant component in SAEO and SPEO was caryophyllene oxide (12.4% and 39.6% respectively). (E)-caryophyllene was another individual constituent with relatively high content in the two oil samples (7.6% and 8.4% respectively).
Caryophyllene oxide is a bicyclic sesquiterpenes, representative for an epoxide derived from the olefin of (E)-caryophyllene. The two structurally similar compounds are common sesquiterpenes in many well-known aromatic plants, such as cloves, basil, hops, cinnamon, and citrus (Nguyen et al. 2017; Sotto et al. 2013). Additionally, essential oils from other Saussurea and Sigesbeckias species including Sa. katochaete Maxim, Sa. parviflora (Poir.) DC., Sa. kansuensis Hand.-Mazz (Wang et al. 2010; Wang 2007), Sa. lappa (Liu et al. 2012b), Si. orientalis, and Si. glabrescens (Makino) (Gao et al. 2018), were also rich in sesquiterpenoids, especially caryophyllene oxide and (E)-caryophyllene. The two sesquiterpenoids are widely present in EOs of many spices and medicinal plants (Sarpietro et al. 2015).
Repellent activity
The results of repellency are listed in Table 2. Repellent activities of SAEO and SPEO against T. castaneum and L. bostrychophila were reported for the first time. Data showed that SAEO, SPEO, caryophyllene oxide, and (E)-caryophyllene had certain repellency against these target insects. Among them, SAEO, SPEO, and caryophyllene oxide in the concentration range of 78.63–3.15 nL/cm2 exerted beneficial repellent effects on T. castaneum, which were comparable with that of DEET at 2 h post-exposure. As for L. bostrychophila, four testing samples of 63.17 nL/cm2 all possessed strong repellency at 4 h post-exposure without statistically significant differences, which could reach the same level of DEET.
Here, (E)-caryophyllene exhibited weak repellency. It was reported to have attractive effects on stored-product insects at lower concentrations before (Liu et al. 2012a, 2012b). Besides applied concentrations of the compound, different insect species would also make different response in assays. Although (E)-caryophyllene was less active against L. bostrychophila in repellent assays, it is acknowledged as a strong repellent among sesquiterpenes against mosquito vectors (Gillij et al. 2008). Notably, caryophyllene oxide exhibited excellent repellency and sustained long duration against T. castaneum and L. bostrychophila. At 4 h post-exposure, its PR value could still reach 92% (class V) against T. castaneum at minimum testing concentration of 3.15 nL/cm2, and it was observed to result in the greatest repellency (100%) against L. bostrychophila at 12.63 nL/cm2. Caryophyllene oxide might play an important role for repellent activities of the total oils. Furthermore, Nararak et al. (2019) covered that caryophyllene oxide produced much stronger irritant and repellent properties against Aedes aegypti (L.) and Anopheles minimus (Theobald) than DEET did, which suggested this compound was promising to be an alternative ingredient in viable repellent formulations for mosquito control.
Thousands of natural plants have been screened as potential sources of botanical repellents, but only a few active substances could exert broad and durable effectiveness comparable with the excellent performance of DEET. Some plant EOs with abundant sesquiterpenes possessed toxicity or repellent activity against aphids, flies, and beetles (Benelli et al. 2018; Wu et al. 2017). The acquisition of rich active substances in EOs is fundamental to the total activity. Optimizing the extractive conditions and sample pre-treatment helps obtain high concentrations of bioactive compounds such as sesquiterpenes including (E)-caryophyllene and caryophyllene oxide in EOs (Fiorini et al. 2019). Additionally, in order to enhance the potency, stability, and target specificity of EOs, nanotechnology for the encapsulation is widely used in natural products to produce nanoformulations (De Oliveira et al. 2014; Hashem et al. 2018). Nanoparticles in combination with active substances are able to greatly improve the quality of botanical products, which make it possible for plant-derived pesticides and repellents to rival those commercially synthetic chemicals.
Bioactivity of a mixture is possibly affected by synergic or antagonistic interactions among various components (Benelli and Pavela 2018). Major components could not directly determine the ultimate repellency of EOs. Minor components might be critical to the bioactivity of multi-component mixtures as well (Pavela 2014). In this work, only two main components caryophyllene oxide and (E)-caryophyllene were assessed for repellency. Evaluation of other sesquiterpenoids remains future work. Furthermore, SAEO and SPEO were performed for repellency while not tested for other mode of action such as fumigant and contact toxicity because of insufficient quantity obtained in this experiment.
Conclusions
The essential oils from aerial parts of Sa. amara and Si. pubescens were mainly composed of sesquiterpenoids and oxygenated sesquiterpenoids. This work confirmed their effective repellent activities against adults of T. castaneum and L. bostrychophila for the first time, and their major component caryophyllene oxide exhibited excellent repellency and sustained long duration against the two stored-product insects. The EOs of Sa. amara and Si. pubescens have potential to be developed into botanical repellents that applied in warehouses and grain stores. The investigation of different modes of action, and possible mutual interactions among various sesquiterpenoids need further work.
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This project was supported by the Yunnan Expert Workstation (2018IC153).
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Li, ZH., Wang, Y., Sun, JS. et al. Repellent activities of essential oils rich in sesquiterpenoids from Saussurea amara (L.) DC. and Sigesbeckia pubescens Makino against two stored-product insects. Environ Sci Pollut Res 26, 36048–36054 (2019). https://doi.org/10.1007/s11356-019-06876-3
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DOI: https://doi.org/10.1007/s11356-019-06876-3