Introduction

The presence of insects in stored grain requires the development and implementation of new naturally occurring agrochemicals for the control and eradication of these harmful pests (Nenaah, 2014). One of the main groups of plague insects, economically important, that affect post-harvest products are Coleoptera beetles. Among them are the red flour beetles, Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae); these beetles act as secondary pests attacking already damaged grains or grain products. They can be found in almost all storage containers of cereals or cereal products, especially in tropical and subtropical climates; they attack corn, wheat, and flour, among others (Jaya, Singh, Prakash, & Dubey, 2014).

Studies of different biological activities, such as repellent, insecticide, antioxidant, antibacterial, and others, show that EOs (essential oils) are useful for controlling pests and other organisms during food storage, due to their high volatility and toxicity (Ukeh & Umoetok, 2011; Kim & Lee, 2014; Celano et al., 2017; Koutsaviti et al., 2018). Compared to some synthetic pesticides, EOs are characterized by minimal effects on human health and the environment, being an extraordinary tool for the agricultural industry (González, Gutiérrez, Ferrero, & Band, 2014).

Pesticides that are used indiscriminately become environmental contaminants causing toxic health effects and pests develop resistance mechanisms against these chemicals (Reis et al., 2016). Due to their bioactive properties, EOs have been considered as an alternative to control insects in stored foods. They are a notable source for developing and implementing new agrochemicals because they are rich in monoterpenes (González et al., 2014; Reis et al., 2016).

EOs are volatile, oily liquids, product of the secondary metabolism of plants (flowers, buds, seeds, leaves, bark, herbs, wood, fruits, and roots). They are comprised of complex mixtures of monoterpenes, sesquiterpenes, phenylpropanoids and other volatile compounds (Sawamura, 2013). They are obtained through distillation by stripping plants through steam or hydro-distillation. They are particularly abundant in some plant families: Conifers, Rutaceae, Umbelliferae, Myrtaceae and Labiatae, and are often localized in specialized histological structures (Koutsaviti et al., 2018; Lee, Annis, Turmaalii, & Choi, 2004). Some EOs have been widely applied in the fields of pharmaceutical, agricultural, sanitary, and cosmetic industries (Silva et al., 2014). They have properties used to kill insects, control pests, and protect stored food crops (Jaya et al., 2014). Furthermore, they are known for their antimicrobial and antioxidant properties, and their use in the food industry has been widely described (Duarte, Luís, Oleastro, & Domingues, 2016; Silva et al., 2014).

Numerous investigations report that monoterpenes and sesquiterpenes had repellent and insecticidal activities (Ukeh & Umoetok, 2011; Kim et al., 2010; Giner et al., 2013). For example, eucalyptol or 1,8-cineole, monoterpenoid present in the Eucalyptus species, was used to control stored grain against Sitophilus oryzae, T. castaneum and Rhyzopertha dominica (Lee et al., 2004) as well as eugenol, citronellal, and geranial on Callosobruchus maculatus and Sitophilus zeamais (Reis et al., 2016).

Swinglea glutinosa is a small shrub belonging to the Rutaceae family; it is native of Asia and is characterized by its abundant foliage and alternate trefoil leaves and inedible fruit, with a strong citrus scent. In Colombia, it is used as hedge in rural and urban areas. The plants and fruits of this species are used in traditional medicine because they deploy several biological properties including antimalarial (Weniger et al., 2001a), antiprotozoal (Weniger et al., 2001b), anti-tubercular (Bueno-Sánchez, Martínez-Morales, Stashenko, & Ribón, 2009), antileishmanial (Rocha, Almeida, Macedo, & Barbosa-Filho, 2005) and insecticidal (Koutsaviti et al., 2018).

One of the important products obtained from S. glutinosa fruit wastes is the EO isolated from citrus peels. The major compounds found in EO are not always responsible for the biological activities; for this reason, identification and detection of all compounds, both majority and minority, becomes necessary. The analytical technique of choice used for this identification is gas chromatography-mass spectrometry (GC-MS) (Stashenko, Jaramillo, & Martínez, 2004).

In this study, we investigated the volatile chemical composition and antioxidant property of EOs isolated from the peel of S. glutinosa grown in Colombia, as well as their repellent and fumigant activities against the T. castaneum using in vitro bioassays. Also, the repellent and fumigant activities of four pure terpenes present in the EOs of S. glutinosa were evaluated.

Material and methods

Reagents

α-Pinene, ascorbic acid (standard substance) and ethanol were purchased from Merck (Darmstadt, Germany); acetone from AppliChem Panreac (Darmstadt, Germany); β-pinene, myrcene, R-limonene, DPPH (1,1-diphenyl-2-picrylhydrazyl) radicals, and C7–C30 n-alkanes were purchased from Sigma-Aldrich (St. Louis, MO, USA); Pirilan from Syngenta S.A. (Colombia) and filter paper from GE Healthcare (Hangzhou, China).

Plant material

The fruits of S. glutinosa (Blanco) Merr were collected in its flowering season in the city of Cartagena, Bolivar, Colombia (Figure 1). The taxonomic characterization of the plant was carried out at the Institute of Biology, School of Natural Sciences, University of Antioquia, Medellin, Colombia by Dr. Francisco J. Roldan Palacios. The vouchers of each plant were deposited in the herbarium as a permanent sample; the identification and code of the plant studied are S. glutinosa, HUA 185262.

Figure 1. Fruits of Swinglea glutinosa (Blanco) Merr. (author’s own source)

Extraction of the essential oil

The Extraction was performed in a Clevenger-type apparatus, according to Jaramillo-Colorado, Martelo, and Duarte (2012). Were used 500 g of fruit peels from S. glutinosa, finely chopped and submerged in boiling water by using conventional heating for two hours. The EO was separated by decantation and then anhydrous Na.SO. was added to the oil. One EO aliquot (30 µL) was diluted in one mL of dichloromethane for gas chromatography analysis.

Chromatography analysis

The EO was analyzed in an Agilent Technologies GC-MS system model 7890A Network GC coupled to a mass selective detector model 5975 (Palo Alto, California, USA) equipped with a split/split-less injection port (230 °C, split ratio 20:1). The mass spectra were obtained by electron-impact ionization at 70 eV energy. GC conditions were as follows: A HP-5MS capillary column (30m x 0.25mm id x 0.25μm df) with 5% phenyl-poly (methyl siloxane) stationary phase was used for the separation of mixtures. The initial oven temperature was 50 °C for 2 min., and then resumed at a rate of 5 °C min^-1. up to 250 °C (5 min.). The carrier gas was helium, with an inlet pressure at the head of the column of 12.667 psi at a rate of 1.172 mL min.^-1, at 50 °C. The mass spectra and Kovàts retention indexes obtained were compared with those reported in the literature (Adams, 2007).

Antioxidant activityAntioxidant activity

Antioxidant activity was evaluated as a measure of the ability to scavenge radicals by reacting with DPPH. (1,1-diphenyl-2-picrylhydrazyl) radicals, potential antioxidants (EO) and ascorbic acid (standard substance). Two milliliters of a 3.6 × 10⁻⁵ M ethanolic solution of DPPH was added to a solution of the tested samples at different concentrations (300, 200, 150, 100, 50, and 10 μg mL^-1). The decrease in absorbance at 517 nm was recorded in an UV−Vis spectrophotometer for 16 min. Antioxidants scavenge the DPPH radical through the donation of hydrogen, which forms the reduced compound, DPPH−H. The color changes from purple to yellow after reduction (a product known as diphenyl picryl hydrazine). Antioxidant activity is expressed as an inhibition percentage, which corresponds to the amount of radical DPPH.offset by the EO, (inhibition percentage of DPPH. radical, % I DPPH.), according to the following equation (Jaramillo-Colorado et al., 2012):

Where Abs. is the absorbance of control (without test sample), and Abs. is the absorbance of the test samples at different concentrations. IC₅₀ (the concentration required to exert 50% of the antioxidant activity) was calculated by linear regression from the percentages of DPPH inhibition. The IC₅₀ results were compared according to Tukey’s statistical method (p < 0.05). Four replications were used for each concentration.

Radical DPPH. was neutralized by the EO from S. glutinosa, and the maximum inhibition percent of DPPH. was 85.8% (2.5 μg mL^-1). A comparison was made with ascorbic acid (a substance used as a reference antioxidant), where the percentage of inhibition against the DPPH. radical was 92.9%. Figure 3 shows that the antioxidant potential of the oil, based on the scavenging activity of DPPH, revealed that a concentration above 142 μg mL^-1 was necessary to reduce 50% of DPPH in the reaction medium.

Wojtunik, Ciesla, and Hajnos (2014) indicated that π bonds are responsible for the chain-breaking antioxidant activity of monoterpenes. They proved that blocking of conjugated double bonds leads to a decrease of the antioxidant property of monoterpenes. Several investigations have reported strong scavenging activity of terpenes found in citrus peel EO as a-pinene, linalool, citronellol, myrcene, γ-terpinene and limonene, among others (Behrendorff, Vickers, Chrysanthopoulos, & Nielsen, 2013; Sawamura, 2013; Singh et al., 2010). As antioxidant compounds donate a proton to the DPPH radical, greater weighting may be given to double bond positions that increase the availability of allylic protons (due to the weaker C-H bond at allyl groups) (Behrendorff et al., 2013).

Insects and bioassays

Adults of T. castaneum used in the experiments were collected seven days after hatching. Bioassays were carried out in the dark in incubators at 28–30 .C and 70–80% relative humidity (r.h) at the Agrochemical Research Laboratory of the University of Cartagena. Oat (Avena sativa) was employed to feed T. castaneum.

Repellent activity

The repellent activity was performed according to (Zhang et al., 2011). The experimental procedure was evaluated by using the area preference method. The EO of S. glutinosa and monoterpenes were dissolved in acetone (0.13, 0.63, 3.15, 15.73, and 78.63 nL cm^-2). Filter paper 9 cm in diameter was cut in half and 500 μL of each concentration was applied separately to half of the filter paper as uniformly as possible with a micropipette. The other half (control) was treated with 500 μL of acetone.

The treated and control half discs were dried at room temperature to allow evaporation of the solvent. Treated and untreated halves were attached using adhesive tape and placed in Petri dishes. Twenty adults (5–7 day old) of T. castaneum were released separately at the center of each filter paper disc. The dishes were then covered and transferred to an incubator at room temperature. Five replications were used for each concentration.

Fumigant activity

The toxic effect from S. glutinosa EO and terpenes were tested on T. castaneum. Filter paper discs (Whatman No. 1, 2-cm in diameter), deposited at the bottom of Petri dish covers (90 x 15 mm), were used. These were impregnated with oil at doses calculated to provide equivalent fumigant concentrations of 500, 350, 250, 150, 50 µg of oil mL^-1 air, respectively. Twenty adult insects (1 to 10 days old) were introduced and tightly capped (replicated four times for each concentration). Pirilan, a commercial pesticide containing methyl pirimiphos (organophosphorus pesticide, 300 μg. mL^-1 air) as an active ingredient, was used as positive control. The mortality percentage was determined after 24 hours from the start of exposure (Prieto, Patiño, Delgado, Moreno, & Cuca, 2011).

Statistical analysis

The results were converted into fumigant percentage and analyzed by ANOVA and Student t tests. Mortality rates were calculated using the statistical formulas of Abbott and Probit to determine the LC₅₀, chi-square values and related parameters (Jaramillo-Colorado, Suarez-López, & Marrugo-Santander, 2019). Biostat a statistical software (Analyst Soft Robust Business Solutions, BioStat Version 2009) was used, with a confidence level of 5%. Four replicates for each analysis were performed.

Results and discussion

Chemical composition of essential oil by gas chromatography analysis

The yield of EO from S. glutinosa was 0.53% (w w^-1). In the GC-MS analysis, 89.5% of the volatile composition could be identified (Table 1). Figure 2 shows a typical chromatogram from S. glutinosa essential oil. Peak identification can be seen in Table 1.

The main components found in the EO from S. glutinosa, were sesquiterpenes: germacrene D (4.8%), nerolidyl acetate (9.8%), and trans-nerolidol (34.6%), and monoterpenes: limonene (5.2%), a-terpineol (6.5%), and b-pinene (8.5%).

These results are different from those found in EO obtained from other regions in Colombia. In the S. glutinosa EO collected in the Cordoba province, the principal components isolated were b-cubebene (26-28%), b-pinene (24-27%) and elixene (10-11%) (Díaz, Arrázola Paternina, Ortega, & Gaviria, 2005). For oil obtained in the city of Bucaramanga, the predominant compounds were β-pinene (49.6%), α-pinene (12%) and β-sabinene (11%) (Bueno-Sánchez et al., 2009). The major constituents of oil derived from fruits collected in Cuba were reported as E-nerolidol (41.3%) and caryophyllene oxide (20.9%) (Pino, Marbot, & Fuentes, 2006).

Figure 2. Typical chromatogram obtained from Colombian Swinglea glutinosa isolated by hydrodistillation and analyzed by gas chromatography coupled with a flame ionization detector (FID) and mass spectrometry (MS) (See Table 1).

The considerable variability in the composition of the EO is probably due to differences in the ecological and climatic conditions, effect of light intensity, altitudes, crop and soil which are directly related to the production of secondary metabolites (Benyelles et al., 2017; Estell, Fredrickson, & James, 2016; Spitaler et al., 2006). Many investigations indicate the existence of the morphological and chemical variability of plant chemotypes, and their vast geographical range, which suggest that species have adapted to new combinations of environmental factors through permanent changes in the genotype, as well as phenotype plasticity (Souza et al., 2018; Andrade et al., 2016; Barra, 2009; Ricciardi et al., 2009)

Repellent and Fumigant activities

EO from S. glutinosa displayed the best repellent activity in higher concentration (15.73 nL cm^-2) after both exposure times, with a repellency percentage of 72±2 % at two hours and 67±2 % at four hours. This was compared to a commercial repellent DEET (N, N-diethyl-toluamide) at the same concentration with an activity of 50±5% for the first two hours and 60±13 % after four hours (Table 2). However, the repellent activity of DEET was highest at 78.63 nL cm^-2 (76% at 2 hours). These results show that the EO of S. glutinosa exhibited a repellent activity close to that of the commercial repellent.

Figure 3. Antioxidant activity from Swinglea glutinosa essential oil measured by the DPPH. method compared to ascorbic acid.

a-pinene exhibited the highest repellent activity against T. castaneum (88%) at 3.15 nL cm^-2 after two hours of exposure and R-limonene deployed a higher repellent activity than those of a-pinene, b-pinene, and myrcene at 15.73 nL cm^-2 (Table 2).

The fumigant toxicities of the EO and four monoterpenes were evaluated against adults of T. castaneum. The results of a data probit analysis, according to the lack of overlap in 95% fiducial limits, showed that pirimiphos- methyl (positive control, LC₅₀=87.4 µg mL^-1 air) was significantly more toxic than S. glutinosa oil (LC₅₀=153.4 μg mL^-1 air) as well as other individual monoterpenes assayed (Table 3). The mean lethal concentrations obtained were as follows: myrcene (LC₅₀=177.8 µg mL^-1 air), (R) - limonene (LC₅₀=189.6 µg mL^-1 air), a-pinene (213.1 µg mL^-1 air), and b-pinene (LC₅₀=227.1 µg mL^-1 air). However, the terpenes exhibited a weaker toxicity compared with pirimiphos- methyl.

Swinglea glutinosa EO, a-pinene, b-pinene, R-limonene and myrcene exhibited high fumigant activity (≥95%) at 350 μg mL^-1 of air, after two hours of exposure, as shown in Figure 4. Significant differences were observed in the number of T. castaneum dead after treatment with S. glutinosa EO (LC₅₀ =153.4 μg mL^-1 air), [F(6.60) =89.54; p < 0.001] for all the doses tested when compared to the pirimiphos control group (LC₅₀ =87.4 μg mL^-1 air), [F(6.60) =12.66; p < 0.001] (Figure 4). The same was observed for the treatments with a-pinene (LC₅₀ =213.1 μg mL^-1 air) [F(6.60) = 57.14; p < 0.001]; b-pinene (LC₅₀ =227.1 μg mL^-1 air L) [F(6.60) = 52.72; p < 0.001]; myrcene (LC₅₀ =177.8 μg mL^-1 air) [F(6.60) =66.64; p < 0.001]; R-limonene (LC₅₀ =189.6 μg mL^-1 air L) [F(6.60) = 36.56; p < 0.001].

Several studies show that the repellent and fumigant properties of EO are associated with the presence of mono and sesquiterpene compounds such as carvacrol, .-cymene, thymol, a-pinene, myrcene (Kim et al. 2010), allyl cinnamate and allyl 2-furoate (Giner et al., 2013), 1,8-cineol, linalool, 2-heptyl acetate, 2-heptanol, citral (Ukeh & Umoetok, 2011), caryophyllene oxide, and caryophyllene (Kiran & Devi, 2007; Kim et al., 2010). The repellent action of some terpenes is similar to those of organophosphorus and carbamate insecticides, which are acetylcholinesterase inhibitors, causing rapid death by respiratory depression (Abdelgaleil, Mohamed, Badawy, & El-arami, 2009; López & Pascual-Villalobos, 2015). For example, limonene is a constituent of citrus EO recommended for the control of scale insects on ornamental plants and agricultural activities in the United States (Hollingsworth, 2005). Terpinen-4-ol, 1,8-cineole, linalool, R-(+)-limonene and geraniol were tested in vapor phase against different stages of Tribolium confusum (Stamopoulos, Damos, & Karagianidou, 2007). Malacrinò, Campolo, Laudani, and Palmeri (2016) reported that R (+)-limonene was able to reach 100% of efficacy or repellent activity on T. castaneum at a concentration of 85 mg L^-1 air. Chaubey (2012) reported that inhibition of acetylcholinesterase enzyme (AchE) activity was observed in S. oryzae adults when fumigated with sublethal concentrations of Zingiber officinale and Piper cubeba EO (α-pinene and β-caryophyllene, respectively) alone or in binary combinations. Kim, Kang, and Park (2013) presented α-pinene as the strongest AchE activity inhibitor followed by β-pinene and limonene. The synergistic or complementary activities of different compounds present in the same oil play a vital role in the final insecticidal and/or repellent activity (Reis et al., 2016).

Figure 4. Fumigant activity from Swinglea glutinosa essential oil and four constituents against Tribolium castaneum at 24 hours after exposure.

Conclusion

We found high antioxidant, repellent and fumigant in vitro activities exhibited by the EO from S. glutinosa (Blanco) Merr., thus increasing interest in the possible application of essential oils as biocides in the control of insects and as protection of products against oxidation. The essential oil from S. glutinosa can be considered a natural source of biocides and antioxidants.

Acknowledgments

The authors acknowledge the support from the Research Group Support Program sponsored by the Vice-Presidency for Research at University of Cartagena; we would also like to thank Jasser Martinez for his technical support.

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