Abstract
The objective of this work was to analyze four essential oils (EOs) from Rhododendron species in China and evaluate their repellent activity against Tribolium castaneum, Lasioderma serricorne, and Liposcelis bostrychophila adults. These four EOs from Rhododendron species, including R. capitatum, R. przewalskii, R. mucronulatum, and R. micranthum, were obtained by hydrodistillation. Major components of four EOs were identified as sesquiterpenoids by GC-MS. The relatively high components included cedrene (22.20%), borneol (36.64%), 4-(2,3,4,6-tetramethylphenyl)-3-buten-2-one (27.74%), and germacrene D (27.60%). Repellent activity of EOs from Rhododendron species was investigated against T. castaneum, L. serricorne, and L. bostrychophila adults for the first time. In this study, EOs had demonstrated their repellent activities against three stored-product insects in 2- and 4-h exposure. The above results can not only provide comprehensive utilization of plant resources of Rhododendron genus but also establish a very good perspective of novel application to control stored-product insects.
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Introduction
The red flour beetle (Tribolium castaneum Herbst), the cigarette beetle (Lasioderma serricorne Fabricius), and the booklouse (Liposcelis bostrychophila Badonnel) are worldwide storage pests with complex eating habits. Because of their rapid breeding speed, strong adaptability, and wide distribution, they have become the most important storage pests of grain, beans, oil, and Chinese medicinal materials (Turner 1994; Garcia et al. 2005; Fardisi and Mason 2013), which bring risk of disease and economical losses to people (Mishra and Dubey 1994; Wei et al. 2012). For a long time, chemical control is the most popular method in controlling pests in storage (Salem et al. 2018). However, long-term use of synthetic chemicals can lead to a number of adverse effects, including possible harm to non-target animals, pollution to the environment, and a threat to human health (Omae et al. 2012; Lashgari et al. 2014; Tago et al. 2014). To solve this problem, it is urgent to replace the chemical control with green and safe pest control methods. Phytochemical insecticides based on EOs (phytoinsecticides) and biological control have been proposed to control storage pests (Desneux et al. 2007; Islam et al. 2010; Miresmailli and Isman 2014). Secondary product of metabolites from EOs is known for their antioxidant and repellent activities, as well as insecticidal properties. (Fang et al. 2010; Polatoğlu et al. 2013; Taban et al. 2017). More importantly, these secondary metabolites from EOs are abundant in natural aromatic plants and possess a series of biodegradable chemical compounds which have advantages of being eco-friendly, having generally low toxicity, and are not easy to make pests resistant to insecticides (Isman 2008; Pavela and Benelli 2016). Thus, botanical insecticides based upon EO have become an increasingly hot researching spot.
Of all the aromatic plant resources, Ericaceae not only has a wide distribution, but also has important economical and medicinal values (Prakash et al. 2007; Wang et al. 2014). Rhododendron genus is the largest and most characteristic genus of the Ericaceae family, including 960 species in the world and 542 species in China. Southwest and South regions of China are the main distribution centers of Rhododendron genus (Fang and Ming 1995). It is worth noticing that the Compendium of Material Medica, a classical masterpiece in Chinese medicine created by Li Shizhen in the Ming Dynasty, recorded that the branches and leaves of the R. molle were poisonous. In the late 1920s, the branches and leaves of R. molle were widely used as pesticide.
In recent years, scholars have begun to study the chemical constituents of Rhododendron species. Research has shown that the strongest active constituent of insecticidal action in R. molle was rhodojaponin-III (Zhong et al. 2010). Since some species of the Rhododendron genus have been reported to have antimicrobial and insecticidal properties (Rezk et al. 2015; Saranya and Ravi 2017), the EOs isolated from the species Rhododendron have been utilized against storage pests. For example, Yang et al. (2011) isolated three bioactive compounds, i.e., 1,4-cineole, 4-pheyl-2-butanone, and nerolidol from the EO of R. anthopogonoides and evaluated their insecticidal activities. The results showed that the three components were effective against Sitophilus zeamais. And the EO of R. thymifolium had obvious insecticidal and repellent activities against T. castaneum and L. bostrychophila (Liang et al. 2016).
At present, researches about some other plants from the Rhododendron species, e.g., R. capitatum, R. przewalskii, R. micranthum, and R. mucronulatum have not been reported to possess repellent activities against storage pests. In this study, repellent activity of the EOs from above four Rhododendron species plants against T. castaneum, L. serricorne, and L. bostrychophila was evaluated for the first time and the results demonstrated that the four EOs from the species Rhododendron have repellent activities against above three storage insects. It was expected to find plant source substances that have the potential to develop into a new type of high-efficiency, green, and low-polluting biological rationality as repellents.
Experiment
Plant materials and extraction
The leaves of four Rhododendron species plants were used in this experiment. The fresh leaves of R. capitatum and R. przewalskii were collected from Tianzhu County of Gansu Province, China. The fresh leaves of R. mucronulatum and R. micranthum were collected from Anshan City of Liaoning Province, China. All the plant samples were identified by Professor Q. R. Liu (College of Life Sciences, Beijing Normal University, Beijing, China) and the voucher specimens in Table 1 were deposited at the herbarium of the Faculty of Geographical Science, Beijing Normal University. The leaves of four Rhododendron species were air-dried and treated into powder. The four EO samples were extracted by hydrodistillation and were stored in dark airtight containers in a refrigerator at 4 °C.
Insects
T. castaneum, L. serricorne, and L. bostrychophila were used in this experiment and were identified by Professor Z. L. Liu (College of Plant Protection, China Agricultural University, Beijing, China). The three types of insects were cultured in a humidity chamber in the dark. The culture temperature is 30 °C and the relative humidity is 70–80%. The red flour beetle and the cigarette beetle were reared in glass containers (0.5 L) containing wheat flour mixed with yeast (10:1, w/w) while the booklouse was bred at a mixture of mike power, yeast, and flour (1:1:10, w/w). The unsexed insects used in all of the experiments were 1–2 weeks old.
GC-FID and GC-MS analysis
In order to determine the chemical constituents of EOs from four Rhododendron species, GC instrument (Agilent 6890N) which was equipped with a flame ionization detector (FID) and coupled to a mass spectrometer (Agilent 5973N) was used in this experiment. The capillary column was HP-5MS (30 m × 0.25 mm × 0.25 μm). The starting temperature of the column was set at 50 °C for 2 min, then raising to 150 °C at the speed of 2 °C/min, and increased to 250 °C at 10 °C/min for 5 min; 250 °C was determined as the final detection temperature and the volume injected was 1 μL of 1% solution (diluted in n-hexane). Helium gas was used as the carrier gas at flow rate of 1.0 mL/min. The retention indices were determined in relation to homologous series of n-alkanes (C5–C36). Most constituents can be identified by comparing their mass spectra with those stored in NIST 05 (Standard Reference Data, Gaithersburg, MD) and Wiley 275 libraries (Wiley, New York, NY) and those published in the literatures (Adams 2001; You et al. 2017). Relative percentages of each component in the EO samples were obtained by averaging the GC-FID peak area (%) reports.
Repellent test
The repellent tests of four EOs from Rhododendron species against the red flour beetle and the cigarette beetle were assessed by using assays on 9-cm diameter Petri dishes (Zhang et al. 2011), while 5.5-cm diameter Petri dishes were used to test booklouse. The samples of four EOs of Rhododendron species were dissolved separately in n-hexane (78.63, 15.73, 3.15, 0.63, and 0.13 nL/cm2) to test the red flour beetle and the cigarette beetle. The filter paper of 9 cm was cut two pieces on average. One piece was given 500 μL n-hexane as blank control, while the other piece was treated with the same volume of testing solution. About 30 s after air drying, two pieces of filter paper were carefully stuck in the bottom of the Petri dish with glue stick. As for booklouse, the EOs of Rhododendron species were dissolved in n-hexane to prepare different concentrations (63.17, 12.63, 2.53, 0.51, 0.10 nL/cm2). The experimental method is similar to the above except for two pieces of filter paper should be given to 150 μL. During each test, 20 insects were placed in the center of the Petri dish and covered with the lid of the Petri dish. The concentration of each text was repeated five times and each text was repeated for five times. At the same time, N,N-diethyl-3-methylbenzamide (DEET), a commercial repellent, was used as a positive control. It was purchased from the National Center of Pesticide Standards (8 Shenliao West Road, Tiexi District, Shenyang 110,021, P. R. China). Counts of the insects present on each trip were made after 2 and 4 h. The calculative formula of the percent repellency (PR) from each volatile was as follows:
Nc represented the number of insects in the control section, and Nt represented the number of insects in the part of the subject. Then the average repellent rate and the SE value were calculated using the variance analysis (ANOVA), Tukey’s test, and SPSS 20.0 for Windows 7 (Sakuma 1998).
Results and discussion
Chemical composition of essential oil
The chemical constituents of EOs by the test of GC-MS were collated in Table 2. The yields of EOs from Rhododendron species ranged from 0.05 to 0.14% (v/w, %). Major compounds of four EOs from Rhododendron species were identified as sesquiterpenoids. There were many similarities among the four species of Rhododendron EOs, but the components with the highest contents were not the same. The major components in R. capitatum and R. przewalskii EOs were cedrene (22.20%) and germacrene D (27.60%) that belonged to the class of sesquiterpenoids. Borneol and 4-(2,3,4,6-tet-ramethylpheny-1)-3-but-en-2-one which belonged to monoterpenoids and aromatic ketone were the major components in R. mucronulatum and R. micranthum EOs with the relative contents of 27.74% and 36.64%, respectively. The main constituents of EO from R. capitatum fresh leaves’ parts which were collected in July were cedrene (22.20%), 1,4,7,-cycloundecatriene,1,5,9,9-tetramethyl-z,z,z- (18.49%), and eremopilene (7.72%), followed by α-gurjunene (5.12%), and selina-3,7(11)-diene (5.40%). However, the above findings were not identical with those that were reported in previous studies. For instance, α-pinene (25.32%) and β-pinene (19.90%) were the main constituents of R. capitatum (also harvested from Tianzhu County, Ganshu Province in September) EO, followed by pyrido[3,4-d]pyrimidin-4(3H)-one, 6,8-dimethyl- (7.45%) (Zhang et al. 2018). And the main components of EO from R. capitatum (leaves and young twigs, collected from Mutual aid Beishan, Qinghai Province) were pinene (0.25%), myrcence (0.69%), 4-phenyl-2-butanone (0.24%), and caryophyllene (0.75%) (Ma et al. 2011). Furthermore, different harvest time, collection places, storage duration, and seasonal factors might have different effects on chemical composition for the same plant EO (Salamon 2007). In addition, different extract parts also resulted difference in chemical components. Previous studies (Meng et al. 2013) showed that the chemical constituent of R. micranthum EOs extracted from leaves and fruits were significantly different. The main components of EO from R. micranthum leaves were ar-turmerone (44.312%), followed by 1-(1,5-dimethyl-4-hexene)-4-methylbenzen (7.048%), and curlone (3.012%), while the major compounds from R. micranthum fruit EO were ar-turmerone (30.12%), 1-(1,5-dimethyl-4-hexene)-4-methylbenzen (4.858%), and α-ilanene (3.826%). In contrast to these reports, the chemical constituents we have researched are fundamentally different from those published. Our analysis of EO compounds in R. przewalskii has never been reported previously. In addition, the above results show that the quality control and standardization about EOs from Rhododendron species need to be further investigated.
Repellent activity
Among various surveyed plants, the Rhododendron genus stands out because its extracts and EOs exhibit antibacterial, antifungal, and anti-inflammatory activities (Qiang et al. 2011; Rezk et al. 2015). Nowadays, the research on extracts and EOs of the Rhododendron genus still relies on published literature (Popescu and Kopp 2013; Liu et al. 2017). There are less researches in the field about the extracts and EOs of Rhododendron genus plants against storage pests. In this paper, we evaluated repellent activity of the four EOs from Rhododendron species including R. capitatum, R. przewalskii, R. mucronulatum, and R. micranthum against three storage pests including T. castaneum, L. serricorne, and L. bostrychophila adults for the first time.
The results of the repellent activity from the EOs of four Rhododendron species were presented in Fig. 1. It demonstrated that all EO samples exhibited repellent activity against three stored-product insects. In the range of 78.63 to 0.13 nL/cm2 in concentrations, the repellent activity exibited a dose response. For example, at the concentration of 78.63 nL/cm2, the repellent activity of EO from R. capitatum against T. castaneum was significantly higher than the concentration of 3.15 nL/cm2 at 4-h exposure. Among these EO samples, at tested concentrations of 78.63, 15.73, 3.15, 0.63, and 0.13 nL/cm2, the volatile oil of R. przewalskii exhibited higher repellency than the positive control of DEET against T. castaneum after 2-h exposure. Even after 4-h exposure, the repellent activity was still relatively strong. The EOs of R. capitatum, R. przewalskii, and R. mucronulatum showed higher repellent activity against L. bostrychophila than the positive of DEET at the testing concentrations of 63.17 and 12.63 nL/cm2 at both 2 h and 4 h after exposure. The EOs of four Rhododendron species had some degree of repellent effects on L. serricorne. In general, the repellent activity of R. micranthum was superior to the other three.
The repellent effects of four EOs from Rhododendron species against insects might be attributed to synergism and antagonism between the main components and minor components (Ntalli et al. 2011). In addition, many chemical compounds have also been reported to have repellent effects on storage pests. For example, borneol, the main component of R. mucronulatum, had obvious repellent effect against L. serricorne (Wu et al. 2014). According to previously reported studies (Guo et al. 2016), the chemical compound β-caryophyllene of R. mucronulatum, at tested dose of 63.17 and 12.63 nL/cm2, the PR of β-caryophyllene reached 100% at 2 h when compared with DEET (94% and 82%), which suggested β-caryophyllene was a strong repellent activity against L. bostrychophila adults. And spathulenol exhibited highly repellent activity against T. castaneum; at tested dose of 78.63, the PR of spathulenol reached 100% (You et al. 2015). Some other relatively high components such as cedrene (22.20%), germacrene D (27.60%), and 4-(2,3,4,6-tetramethylphenyl)-3-buten-2-one (27.74%) may also have good repellent effects against three stored-product insects, which need to be further studied. On the other hand, the different anti-insect mechanisms and nonpersistent volatility of EO samples might cause different repellent effects against stored-product insects. However, there are no reports about the specific mechanism, which need to be further researched.
At present, there are concerns about the safety of DEET and its allergic and toxic effects. To find alternatives for DEET, scientists started to change the form of the natural extracts. Many mixtures of EOs which were extracted from natural plants had been used to prepare microemulsions. The microemulsion-based EOs can not only maintain the original efficacy, but also avoid harm to non-target animals such as some aquatic invertebrates, mammals, and birds (Pavela 2018; Pavela et al. 2019). In a current study, the EO of Eucalyptus globulus was prepared with nano-sized microemulsion that had potential repellency to the extent of DEET and can extend protection time against insects (Navayan et al. 2017). Because four EO samples of Rhododendron species have repellent bioactivity against storage pests, the EOs of Rhododendron species may be considered to prepare nano-sized microemulsion instead of N,N-diethyl-3-methylbenzamide (DEET) as a novel positive control, which will have a bright prospect in the future.
Conclusions
In this study, we evaluated repellent activity of the EOs from four Rhododendron species against three common storage pests for the first time. Results showed that the EOs of four Rhododendron species including R. capitatum, R. przewalskii, R. mucronulatum, and R. micranthum had repellent bioactivity against T. castaneum, L. serricorne, and L. bostrychophila adults. In addition, as secondary metabolites of natural plants, according to their abundant natural resources, these four EOs of Rhododendron species with significant repellent activity might be developed into novel repellents to supply or substitute the heavy application of conventional repellents. Although further detailed investigations are needed, the above results not only provided rationale and evidence for comprehensive utilization of plant resources of Rhododendron genus but also established a very good perspective of novel application in control of stored-product insects.
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This project was supported by the Science and Research Project of the Education Department of Liaoning Province (LYB201608).
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Bai, L., Jiao, ML., Zang, HY. et al. Chemical composition of essential oils from four Rhododendron species and their repellent activity against three stored-product insects. Environ Sci Pollut Res 26, 23198–23205 (2019). https://doi.org/10.1007/s11356-019-05577-1
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DOI: https://doi.org/10.1007/s11356-019-05577-1