Hostname: page-component-7b9c58cd5d-g9frx Total loading time: 0 Render date: 2025-03-16T06:14:54.061Z Has data issue: false hasContentIssue false

Assessment of the potential of non-thermal atmospheric pressure plasma discharge and microwave energy against Tribolium castaneum and Trogoderma granarium

Published online by Cambridge University Press:  26 March 2021

Abeer O. Abotaleb*
Affiliation:
Stord Product Pest Department, Plant Protection Research Institute, Agriculture Research Center, Giza, Egypt
Naglaa F. Badr
Affiliation:
Zoology Department, Faculty of Science, Al-Azhar University, Cairo, Egypt
Usama M. Rashed
Affiliation:
Physics Department, Faculty of Science, Al-Azhar University, Cairo, Egypt
*
Author for correspondence: Abeer O. Abotaleb, Email: dabeeromar@gmail.com
Rights & Permissions [Opens in a new window]

Abstract

This study was carried out to investigate the efficacy of the non-thermal atmospheric pressure plasma produced with dielectric barrier discharge (APPD) using air as a processing gas and microwave energy to control Tribolium castaneum and Trogoderma granarium adults and larvae in wheat grains. Insects’ mortality was found to be power and time-dependent. The results indicated that non-thermal APPD and the microwave have enough insecticidal effect on the target pests. From the bioassay, LT50's and LT90's levels were estimated, T. granarium larvae appeared more tolerant to non-thermal APPD and the microwave energy than adults 7 days post-exposure. The germination percentage of wheat grains increased as the time of exposure to the non-thermal APPD increased. On the contrary, the germination percentage of wheat grains decreased as the time of exposure to the microwave increased. In addition, changes in antioxidant enzyme activities, catalase (CAT), glutathione S-transferase (GST) and peroxidase, in adults and larvae were examined after 24 h post-treatment to non-thermal APPD at 15.9 W power level, which caused 50% mortality. The activity of CAT, GST and lipid peroxide in the treated larvae showed a significant increase post-exposure to the non-thermal APPD at 15.9 W power level. On the other hand, no significant change in GSH-Px activity was observed. Reductions in the level of glutathione (GSH) and protein content occurred in treated larvae in comparison with the control.

Type
Research Paper
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

Introduction

Stored-product insects are a recurrent problem in retail stores, where they damage and contaminate food products. Tribolium castaneum (Coleoptera: Tenebrionidae) and Trogoderma granarium (Coleoptera: Dermestidae) feed on various stored products such as flour and cereals. Tribolium castaneum is also highly tolerable to humidity as low as 11% and reduces the quality and quantity of the infected products (FAO, 2008). Potentially, it has an important impact on public health since it produces as irritants and repellents several varieties of substituted benzoquinone compounds that are highly reactive and toxic (Li et al., Reference Li, Lehmann, Weißbecker, Ojeda Naharros, Schütz, Joop and Wimmer2013). The beetles emit an unpleasant odor and can expedite the growth of the fungus in the contaminated products (Rustamani et al., Reference Rustamani, Khatri, Sultana and Laghari2014).

The khapra beetle, T. granarium, is a serious post-harvest pest of grain and cereal products in many tropical and subtropical regions of the world and has been considered as one of the 100 most invasive pests in the world (Lowe et al., Reference Lowe, Browne, Boudjelas and de Poorter2000). This species is a noxious stored product insect that is listed as a quarantine species by the European and Mediterranean Plant Protection Organization (EPPO) and others (Myers and Hagstrum, Reference Myers, Hagstrum, Hagstrum, Philips and Cuperus2012). Its undeniable economic importance relies on its ability to cause huge physical and quality losses in the stored grains by feeding and increasing the temperature of the storage environment making them liable to be invaded by some other pests including fungi and bacteria (Özberk, Reference Özberk2018). It has been estimated that an infestation level of 75% damaged grains by T. granarium larvae in wheat grains and some other cereals causes a considerable reduction in total protein and carbohydrate and other direct and indirect damage to the grain (Ahmedani et al., Reference Ahmedani, Haque, Afzal, Aslam and Naz2009).

Control of this kind of insects relies heavily on the use of fumigants, which has led to problems such as environmental pollution, increasing costs of the application, pest resurgence and resistance and hazard effects on non-target organisms in addition to direct toxicity to users (Benhalima et al., Reference Benhalima, Chaudhry, Mills and Price2004; Kumar et al., Reference Kumar, Mohapatra, Kotwaliwale and Singh2016).

Non-thermal atmospheric pressure plasma discharge (APPD) is a specific type of plasma that is <40°C at the point of application (Nasr et al., Reference Nasr, Zinhoum and Lotfy2020). The non-thermal atmospheric pressure plasma is a promising technology that is simple to set up, easy to operate and economical and it can be considered a safe physical method for the disinfection of agricultural products after harvest (Tyata et al., Reference Tyata, Subedi, Shrestha and Baral2012). As a processing environment, non-thermal APPD offers unique advantages of high chemical reactivity, low power consumption, high energy efficiency and low gas temperature without the need for complicated vacuum systems (Zhou, Reference Zhou2019). It is a mixture of atoms, molecules, ions, and electrons. Recently, the efficacy of non-thermal APPD types against insects, Sitophlus granarius, Plodia interpunctella, Ephestia kuehniella and T. castaneum, was evaluated (Mishenko et al., Reference Mishenko, Malinin, Rashkovan, Basteev, Bazyma, Mazalov and Kutovoy2000; Abd El-Aziz et al., Reference Abd El-Aziz, Mahmoud and Elaragi2014; Mohammadi et al., Reference Mohammadi, Imani, Dorranian, Tirgari and Shojaee2015). Other plasma species, atoms, metastable, and gaseous radicals can also have a pesticidal effect. Nevertheless, these plasmas should be non-thermal, therefore combining a low gas temperature close to the ambient, with high electron temperature, the electrons with high energies being able to sustain the generation of active chemical species including reactive oxygen species (ROS) and nitrogen species (Carpen et al., Reference Carpen, Chireceanu, Teodorescu, Chiriloaie, Teodoru and Dinescu2019; Zhou, Reference Zhou2019). Operation in the air reduces the costs when compared to the use of noble gases and the dielectric barrier discharge (DBD) system is a promising choice in order to adopt the non-thermal APPD technology for the management of stored-product pests (Kim et al., Reference Kim, Yun, Jung, Jung, Jung, Choe and Jo2011).

Microwaves are a part of the spectrum of the electromagnetic radiation and comprising frequencies ranging from 300 MHz to 300 GHz corresponding to a wavelength from 1 m to 1 mm (Abdelghafar, Reference Abdelghafar2015). Microwave disinfestation is a physical method that can be used to control insects in stored cereals and cereal products (Vadivambal et al., Reference Vadivambal, Jayas and White2006). Moreover, microwave heating is based on the transformation of alternating electromagnetic field energy into thermal energy by affecting polar molecules of a material (Chen et al., Reference Chen, Chen, Chen, Zhang and Zheng2019). Whereas they are especially useful because of their ability to penetrate common, non-conducting materials (Bhattacharya and Basak, Reference Bhattacharya and Basak2017). The use of microwaves to kill insects is based on the dielectric heating effect produced in grain which is a relatively poor conductor of electricity (Vadivambal et al., Reference Vadivambal, Jayas and White2007). Microwave quarantine method seems to have great potential as an alternative method of killing insects in stored grain because of several advantages such as the control of all developmental stages of storage pests, having no chemical residues on the food product, having minimal impact on the environment. Insects are unlikely to develop resistance to this treatment and providing rapid heating (Wang and Tang, Reference Wang and Tang2001; Karabulut and Baykal, Reference Karabulut and Baykal2002). Some authors are unanimous in affirming that the ionizing radiation can sterilize or kill insects of the order Coleoptera pests of stored grains (Vadivambal et al., Reference Vadivambal, Jayas and White2006, Reference Vadivambal, Jayas and White2007; Manickavasagan et al., Reference Manickavasagan, Alahakoon, Al-Busaidi, Al-Adawi, Al-Wahaibi, Al-Raeesi and Jayas2013; Abd El-Raheem and Said, Reference Abd El-Raheem and Said2016).

The main objective of this study was to investigate the possible use of non-thermal APPD with air as the working gas and microwave energy as stressor agents necessary for the control of T. castaneum and T. granarium adults and larvae in wheat grains, besides investigating their effect on the viability of wheat grains (in terms of wheat germination). Furthermore, the present study was carried out to investigate the antioxidative defense system in T. castaneum and T. granarium adults and larvae that occur under non-thermal plasma treatments.

Materials and methods

Insects culture

Tribolium castaneum and T. granarium adults and larvae were reared on Egyptian wheat variety Sakha 69 obtained from an already existing culture at the research laboratory of Stored Products Department, Plant Protection Research Institute, Doki, Giza, Egypt. To prepare immature individuals for use in each of the assays, the following procedure was performed. Tribolium castaneum adults were added to glass jars containing wheat grains and wheat flour, then given 48 h to settle, mate, and lay eggs, before being removed using a #25 sieve. Larvae were used in experiments 2.5–3 weeks after the removal of adults (Pranavi et al., Reference Pranavi, Prasad and Lakshmipathi2016). A similar procedure was performed for T. granarium larvae, with adults given 48 h to reproduce before being removed. Given that the larvae may go through supernumerary molts based on food availability and density, it is difficult to determine instars, so T. granarium larvae were classified as large, given 7–8 weeks to develop, or small, given 3–4s week, which conforms to prior size classification schemes for Trogoderma spp. (Domingue et al., Reference Domingue, Morrison, Yeater and Myers2020). Insects were reared under controlled conditions set at 30 ± 2°C, with the relative humidity of 60 ± 5%.

Non-thermal APPD treatment

The samples were treated with a non-thermal plasma system developed at the Department of Physics, Faculty of Science, Al-Azhar University as illustrated in the schematic diagram of DBD cell used as a stress for the control of T. castaneum and T. granarium adults and larvae (fig. 1). The DBD reactor consisted of two parallel plate electrodes. The upper electrode is an Al-sheet of dimensions 25 × 25 cm2 pasted on the dielectric glass plate of thickness 1.5 mm and the lower electrode was a stainless-steel plate of the same dimensions. The gap distance between the dielectric glass plate and the lower electrode is 2–3.5 mm. Plasma discharges were generated by a 25 kV/30 mA AC power supply of 50 Hz frequency, which is connected to the upper electrode, while the lower electrode is connected to earth through a resistor R of 100 Ω or a capacitor C of 3.35 μf. The voltage across discharge electrodes was measured using a resistive potential divider (1:1000) which was connected in parallel with the discharge electrodes. The discharge current has been measured by measuring the voltage drop across the resistor R through a digital storage two-channel oscilloscope (GWinsTEX GDs-1072-u, 70 MHZ). The dissipated power during the discharge has been estimated using a capacitor C to calculate charge flow through the reactor. The temperature reached by the samples during treatments was evaluated using a thermocouple inserted inside the grain samples. The thermocouple reading was performed at the end of each treatment. Due to the use of a non-thermal plasma source and the power conditions used here, temperatures 40–45°C have been determined on the samples due to the lower AC power supply of 50 Hz frequency.

Figure 1. The schematic diagram of DBD cell used as a stress for the control of T. castaneum and T. granarium adults and larvae.

DBD pulses are the visually uniform glow-like discharge plasma consisting of strong filamentary discharges on the surface over the gap between the electrodes that are typical of filamentary barrier discharges. For the duration of the rising and falling voltage half-cycles, the current directions (positive or negative) are distinct. The accumulation of charges on the surface of quartz creates an inverse electrical field along the surface, leading to the quenching of the relatively strong filamentary discharges. The elementary discharges are distributed randomly over the quartz surface and are getting stronger at an increasing gas voltage, resulting in the visually uniform plasma. More discharge channels can be generated by increasing applied voltage as illustrated by the current-voltage waveform for atmospheric pressure air plasma discharge at about (a) 9 KV and (b) 10 KV applied voltage (fig. 2a, b) (Bhesh and Raju, Reference Bhesh and Raju2019). The increase of voltage leads also to the reduction of the duration of micro-discharges, probably due to the higher electric field. At a dielectric surface, the micro-discharge channels spread into surface discharges covering a much larger region than the original channel diameter. Moreover, the discharge power also could be determined by a Lissajous figure as illustrated by the air DBD plasma at about 9, 10, and 11 KV applied voltages (fig. 3); they are an important technique for the electrical characterization of DBDs and can be created by plotting the charge transferred during the discharge and applied voltage (Kostov et al., Reference Kostov, Nishime, Hein and Toth2013). The insect's samples were placed in the gap between two electrodes under atmospheric pressure air and the DBD system is operated using air as a processing gas (fig. 1). Samples of 10 g of wheat grains consisted of 25 larvae and 25 adults for both insects and separately for each treatment in small cloth bags. The insects were exposed to 5.4, 10.15, and 15.9 W for 3, 5, 10, 15, 20, 30, 60, 90, 120, and 150 s for T. castaneum and T. granarium adults and larvae. Three replications were conducted for each insect and control. After treatment, the packaging material containing insect and wheat grains was kept in the incubator under constant conditions (30 ± 1°C, 60 ± 5% RH). Observations on the mortality of adults and larvae were carried out at 24 h and 7 days post-exposure. Mortality percentages were calculated and corrected according to Abbott formula for natural mortality in untreated controls (Abbott, Reference Abbott1925).

Figure 2. Current voltage waveform for atmospheric pressure air plasma discharge at about (a) 9 KV and (b) 10 KV applied voltage.

Figure 3. Lissajous figures of air DBD plasma at about 9, 10, and 11 KV applied voltages.

Microwave treatment

The microwave system (Model MS23K3513AK, 230 V-50 HZ-800 W-2450 MHZ) was used. Samples of 10 g of wheat grains consisting of 20 larvae and 20 adults for both insects were put in Petri dishes. Samples were exposed to 100, 180, and 300 W for 20, 30, 60, 90, 120, and 150 s for T. castaneum and T. granarium adults and larvae. Three replications were conducted for each insect and control. After treatment, the treated samples were packed in small cloth bags and kept in the incubator under constant conditions (30 ± 1°C, 60 ± 5% RH). Observations on the mortality of adults and larvae were carried out at 24 h and 7 days post-exposure. Mortality percentages were calculated and corrected according to Abbott formula for natural mortality in untreated controls Abbott (Reference Abbott1925). The temperatures of the wheat kernels during treatment were monitored using an electronic probe thermometer. The thermometer reading was performed at the end of each treatment. Temperatures 60–90°C have been determined on the samples due to the treatment of microwave.

Wheat grain germination test

The viability of wheat grains post-treated with non-thermal atmospheric pressure plasma and microwave energy was carried out to find the effect of the non-thermal APPD and microwave energy on germination of post-treated wheat grains to LT50's and LT90's levels used in present work as food for the experimental insects at 15.9 and 300 W power level for non-thermal APPD and microwave energy, respectively. The treated seeds were placed on the filter paper in 9 cm Petri dishes and 10 ml of distilled water was added into each dish to create germinating conditions. After that, these samples were incubated in a light incubator at the temperature of 25°C. During the germination and growth, 5 ml of distilled water was added daily to each Petri dish to keep sufficient moisture for germination. The germination percentage was recorded after 7 days.

Biochemical tests

Non-thermal plasma in terms of LT50 was chosen for studying biochemical effects on T. castaneum and T. granarium adults and larvae. Adults and larvae were selected 24 h post-exposure to 15.9 W power level of non-thermal plasma, which caused 50% mortality. Glutathione S-transferase (GST), catalase (CAT), peroxidase, phenoloxidase, lactate dehydrogenase (LDH) were determined according to the methods of Ishaaya (Reference Ishaaya1971), DGCK (1972), Habig et al. (Reference Habig, Pabst and Jakoby1974), Hammerschmidt et al. (Reference Hammerschmidt, Nuckles and Kuc1982), and Aebi (Reference Aebi1984), respectively. Protein contents in adults and larvae extracts were determined using the method described by Bradford (Reference Bradford1976).

Statistical analysis

For statistical analysis, the average percent mortalities of the tested insects were calculated and corrected using Abbott's formula (Abbott, Reference Abbott1925). To get the best fitting of the obtained results, both exposure times and tested powers were transformed to log values (LN (value + 1)). Hence the statistical model becomes Y = a ± b 1 LN (Exposure time + 1) ± b 2 LN (Power + 1). Obtained results were analyzed using Proc Reg in SAS (Anonymous, 2003). This is considered as Multiple Regression Model (determination of the significant effect of multiple factors on one aspect). R 2 values presented the goodness of fitting, while the P values presented the significant probability of the tested factors (i.e. exposure times and tested powers) over 24 h and 7 days. On the other hand, for estimating the expected exposure time to cause 50 and 90% mortality, each set of data (under each tested power for each stage belonging to each pest) that obtained mortality data were fitted to linear relation as Y = a ± b (LN exposure time + 1). Hence 50 and 90% mortality were estimated using the following equations: (LN exposure time + 1) = (50−a)/b and (LN exposure time + 1) = (90−a)/b (for 50 and 90%, respectively). The inverse of obtained values (−1) (i.e. exp values−1) was considered to present the expected exposure times to case 50 and 90% mortality, respectively. To elucidate the general differences between the two pests, stages, and inspection times factorial analysis was conducted using Proc ANOVA in SAS. Means were compared by Tukey's HSD (P = 0.05 level) in the same program. Obtained data from biochemical and germination tests were analyzed as one/two-way ANOVA, in the same program.

Results

The effect of non-thermal APPD on the survival of T. castaneum and T. granarium adults and larvae

The effect of non-thermal APPD produced with DBD using air as a processing gas on the survival of adults and larvae of T. castaneum 24 h and 7 days post-exposure to different powers for various time periods is shown in table 1. Non-thermal APPD caused 13.3 and 20.0% mortality to T. castaneum adults and larvae, respectively, at 5.4 W power level for an exposure time of 3 s which is increased by increasing the power level to reach 18.3, 25.0% and 20.0, 33.3% mortality at the power levels 10.15 and 15.9 W, respectively, for the exposure time 3 s to T. castaneum adults and larvae, respectively. Moreover, the mortality percentage of T. castaneum adults and larvae was increased by increasing the exposure times and power level to reach 80.0 and 83.3% at 5.4 W power level for an exposure time of 150 s, respectively, which amount to 86.7 and 91.7% for T. castaneum adults and larvae at 15.9 W power level of non-thermal APPD, respectively (table 1). The exposure time of 120, 90, and 60 s to non-thermal APPD at 5.40, 10.15, and 15.90 W power level caused complete mortality to T. castaneum larvae, respectively, 7 days post-exposure. Non-thermal APPD caused 35.0, 40.0, and 58.3% mortality at 5.40, 10.15 and 15.90 W power levels which increased by increasing the exposure times and power level to reach 95.0 and 98.3% mortality to T. castaneum adults, respectively, 7 days post-exposure. Similar conclusions were secured in the case of the mortality of T. granarium adults and larvae. The effect of non-thermal APPD produced with DBD using air as a processing gas on the survival of adults and larvae of T. granarium 24 h and 7 days post-exposure to different powers for various time periods is shown in table 2. The mortality percent was 22.7 and 18.7% at the 3 s, 5.4 W power level for adults and larvae, respectively, 24 h post-exposure to the non-thermal APPD, while it reached 24.0, 20.0% and 25.30, 24.60% at the 3 sec, 10.15 and 15.9 W power level for adults and larvae, respectively, 24 h post-exposure to the non-thermal APPD. Additionally, the mortality percentage of T. granarium adults and larvae was increased by increasing the exposure times and power level to reach 77.3 and 86.7% at the 150 s, 5.4 W power level for adults and larvae, respectively, 24 h post-exposure to the non-thermal APPD, whereas it reached 88.0, 93.3% and 92.0, 97.3% at the 150 s, 10.15 and 15.9 W power level for adults and larvae, respectively, 24 h post-exposure to the non-thermal APPD. While 90.0, 60.0, and 30.0 s exposure to non-thermal APPD caused complete mortality to T. granarium adults at 5.4, 10.15, and 15.9 W power level, respectively, 7 days post-exposure. In addition, non-thermal APPD caused 30.7, 34.7, and 38.7% mortality at 5.4, 10.15, and 15.9 W power levels which increased by increasing the exposure times and power level to reach 86.7, 93.3, and 97.3% mortality to T. granarium larvae, respectively, 7 days post-exposure.

Table 1. Effect of non-thermal APPD using air as a processing gas on the percentage mortality (mean ± SE) of T. castaneum adults and larvae 24 h and 7 days post-exposure to different powers at various time periods (sec)

Table 2. Effect of non-thermal APPD using air as a processing gas on the percentage mortality (mean ± SE) of T. granarium adults and larvae 24 h and 7 days post-exposure to different powers at various time periods (sec)

Determination of the significant effect of exposure times and tested power levels of the non-thermal APPD factors on the mortality percent of T. castaneum and T. granarium adults and larvae is presented in table 3. After 24 h post-exposure, both factors (time and power level) were highly significant (P < 0.0001, with R 2 = 0.93, 0.98 and 0.97, 0.96, respectively) to non-thermal APPD. Whereas after 7 days, the main factor that affects the mortality percent of T. castaneum and T. granarium adults and larvae was attributed to the exposure time (P < 0.0001, with R 2 = 0.9, 0.8, and 0.7), respectively.

Table 3. Determination of the significant effect of exposure times and tested power level factors on the mortality percent of T. castaneum and T. granarium adults and larvae after 24 h and 7 days post-exposure to non-thermal APPD using air as a processing gas

Results of the factorial analysis for the general trend between the two pests, stages, and the time of exposure are shown in table 4. A highly significant effect was recorded due to the exposure time on T. castaneum and T. granarium mortality (F 1,248 = 151.05 and P = 0.0001). The most influential factor that had a massive effect was the exposure time while a non-significant effect was recorded due to the pest and the stages (F = 0.72, P = 0.39 and F = 0.14, P = 0.71), respectively.

Table 4. Factorial analysis for the general trend between the two pests, stages, and inspection times post-exposure to non-thermal APPD

Means with the same letter are not significantly different.

The effect of microwave energy on the survival of T. castaneum and T. granarium adults and larvae

The mortality percent of T. castaneum adults and larvae 24 h and 7 days post-exposure to different powers of microwave energy for various time periods is shown in table 5. The percentage mortality was 20.0% to T. castaneum adults and larvae, respectively, at 100 W power level for an exposure time of 30 s which increased by increasing the power level to reach 23.3, 76.7% and 46.7, 66.7% mortality at the power levels 180 and 300 W, respectively, for the exposure time 30 s to T. castaneum adults and larvae, respectively. The exposure time of 90, 120, and 150 s to microwave energy at 300 W power level caused complete mortality to T. castaneum adults 24 h post-exposure. While the exposure time of 150 s to microwave energy at 180 W power level caused complete mortality to T. castaneum larvae 24 h post-exposure. Moreover, the mortality percentage of T. castaneum adults and larvae was increased by increasing the exposure times and power level of the microwave energy to reach 100% at 300 W power level for an exposure time of 90 and 60 s for T. castaneum adults and larvae, respectively, 7 days post-exposure. Similar results were obtained in the case of the mortality of T. granarium adults and larvae post-exposure to microwave energy 24 h and 7 days post-exposure to different powers for various time periods as shown in table 6. The mortality percent was 23.3 and 20.0% at the 60 s, 100 W power level for adults and larvae, respectively, 24 h post-exposure to the microwave energy, while it reached 100% at the 120 s, 180 W power level for adults and 100% at the 150 s, 300 W power level for larvae 24 h post-exposure to the microwave energy. Furthermore, the mortality percentage of T. granarium adults and larvae was increased by increasing the exposure times and power level of the microwave energy to reach 100% at 180 and 300 W power level for an exposure time of 120 and 150 s for T. castaneum adults and larvae, respectively, 7 days post-exposure.

Table 5. Effect of microwave energy on the percentage mortality (mean ± SE) of T. castaneum adults and larvae 24 h and 7 days post-exposure to different powers at various time periods (sec)

Table 6. Effect of microwave energy on the percentage mortality (mean ± SE) of T. granarium adults and larvae 24 h and 7 days post-exposure to different powers at various time periods (sec)

Determination of the significant effect of exposure times and tested power levels of the microwave energy factors on the mortality percent of T. castaneum and T. granarium adults and larvae is presented in table 7. Both factors (time and power level) that affect the mortality percent of T. castaneum and T. granarium adults and larvae were highly significant (P < 0.05, with R 2 = 0.791, 0.84 and 0.798, 0.746, respectively) and (P < 0.05 with R 2 = 0.82, 0.87 and 0.95, 0.78), respectively, 24 h and 7 days post-exposure to the microwave energy.

Table 7. Determination of the significant effect of exposure times and tested power level factors on the mortality percent of T. castaneum and T. granarium adults and larvae after 24 h and 7 days post-exposure to microwave

Results of the factorial analysis for the general trend between the two pests, stages, and the time of exposure are shown in table 8. A highly significant effect was noted due to the time on T. castaneum and T. granarium mortality after 24 h and 7 days post-exposure to the microwave energy (F 1,167 = 8.59 and P = 0.0039). The most influential factor that had a massive effect was the exposure time while a non-significant effect was recorded due to the pest and the stages (F = 0.93, P = 0.3369 and F = 1.28, P = 0.26), respectively.

Table 8. Factorial analysis for the general trend between the two pests, stages, and inspection times post-exposure to microwave energy

Means with the same letter are not significantly different.

The expected exposure time to cause 50 and 90% mortality for T. castaneum and T. granarium adults and larvae post-exposure to non-thermal APPD and microwave at different power levels after 24 h and 7 days post-exposure is presented in tables 9 and 10. The expected exposure time to cause 50 and 90% mortality values decreased with increased exposure time and power level for both insects after 24 h and 7 days post-exposure to non-thermal APPD and microwave powers. The expected exposure time to cause 90% mortality values for T. granarium larvae was greater than those for the adult stage of the same insect and greater than those of T. castaneum adults and larvae at the same power levels after 7 days of exposure. Trogoderma granarium larvae were the most tolerant life stage to non-thermal APPD and required 161.88, 115.13, and 82.59 s to achieve 90% mortality across the 5.4, 10.15 and 15.9 W power levels, respectively, after 7 days of exposure to non-thermal APPD. Also T. granarium larvae required 10650.44, 388.14, and 103.17 s to achieve 90% mortality at 100, 180, and 300 W power levels, respectively, after 7 days of exposure to microwave energy.

Table 9. The expected exposure time (sec) caused 50 and 90% mortality for T. castaneum and T. granarium adults and larvae post-exposure to non-thermal APPD using air as a processing gas at different powers after 24 h and 7 days post-exposure

Table 10. The expected exposure time (sec) caused 50 and 90% mortality for T. castaneum and T. granarium adults and larvae post-exposure to microwave at different powers after 24 h and 7 days post-exposure

The present study investigated the effect of non-thermal APPD application at 15.9 W and microwave energy at 300 W as a power level on the germination of post-treated wheat grains at LT50's and LT90's levels used in the present study (table 11). Our results showed that, even though the germination percent increased as the time of exposure increased, the germination percentage of wheat grains post-exposure to LT50 of tested insects significantly decreased post-exposure to non-thermal APPD 37.0, 29.0, 37.0, 32.0% for LT50 to T. granarium and T. castaneum adults and larvae, respectively, compared to control 63.0% (P < 0.05). On the contrary, the germination percentage of wheat grains post-exposure to non-thermal APPD at LT90 generally, there were non-significantly differences in germination percent after non-thermal APPD treatment 71.0, 67.0, 55.0, and 64.0% at LT90 for T. granarium and T. castaneum larvae and adults, respectively, compared to 63.0% for control (P > 0.05). Our result showed that the plasma grain treatment for an appropriate time of 1.9–3.1 min (112.55–182.97 sec) improved the germination. A decrease of germination started beyond 2.08 min (124.61 sec) was only observed 24 h post-exposure to non-thermal APPD but still insignificant with control (P > 0.05).

Table 11. Effect of non-thermal APPD at 15.9 W and microwave energy at 300 W on the germination% of wheat grains post-exposure to lethal exposure times at the 50 and 90% level of T. castaneum and T. granarium adults and larvae

Means followed by the same letter are not significantly different using Tukey's HSD test (P = 0.05).

The results of the germination test conducted on wheat grains post-exposure to microwave energy (300 W power level) at LT50's and LT90's levels induced the germination percent decreased as the time of exposure increased table 11. The germination percentage of wheat grains post-exposure to LT50 of tested insects significantly decreased post-exposure to microwave power (300 W) to 52.0, 57.3, and 38.0% for LT50 to T. castaneum and T. granarium adults and larvae, respectively, compared to control 78.0% (P < 0.05). Only a non-significant decreased (66%) was observed post-exposure to microwave power (300 W) for LT50 to T. castaneum larvae compared to control 78.0% (P < 0.05). Moreover, the germination percentage of wheat grains post-exposure to LT90 significantly decreased after microwave treatment to 4, 13, 7, and 0% at LT90 for T. castaneum and T. granarium larvae and adults, respectively, compared to 78% for control (P < 0.05).

Changes in antioxidant enzyme activity in T. castaneum and T. granarium adults and larvae were examined 24 h after exposure to 15.9 W of non-thermal plasma, which caused 50% mortality as shown in table 12. In the present study, the results of measurements of CAT activity showed an increase in its level and was significantly higher in larvae of both insects and adults of T. granarium compared to that in the control (P < 0.05). The CAT activity showed no significant changes among T. castaneum adults (P > 0.05) compared to that in the control.

Table 12. Changes in antioxidant enzyme activity and total proteins (mean ± SE) in T. castaneum and T. granarium adults and larvae 24 h after exposure to lethal exposure times 50% level at 15.9 W power level of non-thermal APPD using air as a processing gas

Means followed by the same letter are not significantly different using Tukey's HSD test (P = 0.05).

The results of measurements of GST activity showed a significant increase in the activity of GST in adults’ stage of both insects compared to that in the control (P < 0.05). While a significant decrease in the activity of GST in larval stages of both insects is observed compared to control (P < 0.05) after 24 h of non-thermal APPD application.

Data presented in table 12 revealed that a significant decrease in peroxidases activity was recorded in all stages in both insects after 24 h of non-thermal APPD application than in controls (P < 0.05).

By comparing the levels of LDH and phenol oxidase (PO) in both T. castaneum and T. granarium in larval and adult stages after 24 h of non-thermal APPD application, it was found that in LDH and PO levels significantly changed in adult stages of both insects and the larval stage for T. granarium compared to control (P < 0.05). Whereas there were no significant differences in the activity of LDH and PO levels in the larvae of T. castaneum treated with non-thermal APPD opposed to controls (P > 0.05) 24 h post-exposure.

On the other hand, when comparing the total protein levels in T. castaneum and T. granarium post-exposure to 24 h of non-thermal APPD application, it was found that the total protein significantly decreased in T. castaneum in both adults and larval stages compared to control (P < 0.05) (table 12). However, there was a non-significant decrease in the total protein levels in T. granarium in both adults and larvae stages treated with non-thermal APPD as opposed to controls (P > 0.05) 24 h post-exposure.

Discussion

Various insects cause quantitative and qualitative losses in stored products every year. Chemical pesticides are widely used to control stored product pests (Konradsen et al., Reference Konradsen, Van Der Hoek, Cole, Hutchinson, Daisley, Singh and Eddleston2003). Concerns about resistance to insecticides, as well as their environmental impact, have stimulated researchers to find out an alternative pest control method. Results obtained revealed that non-thermal APPD and different powers of microwave energy showed an effective method against the T. castaneum and T. granarium adults and larvae at various treatments and the mortality percentage which is investigated with independent variables: applied power and exposure time. The results indicated that there was a positive relationship between mortality rates of T. castaneum and T. granarium and both power levels and exposure times of non-thermal APPD and microwave. The mortality percent was found to be power and time-dependent 24 h and 7 days post-exposure, i.e. increased with increasing applied power and with increasing exposure treatment time. In case of the microwave, the main reason for this positive relationship could be due to the increase in the frequency oscillation of the water molecules in the body of treated insects (Zhao et al., Reference Zhao, Qiu, Xiong and Cheng2007; Valizadegan et al., Reference Valizadegan, Pourmirza and Safaralizadeh2009). Vadivambal et al. (Reference Vadivambal, Jayas and White2006) reported that the use of microwaves is based on the dielectric heating effect produced in grain, which is a relatively poor conductor of electricity. An attractive feature of insect control using microwave energy is that the insects are heated at a faster rate than the product they infest because of the high moisture content of insects. So, it is possible to heat the insects to a lethal temperature because of their high moisture content while leaving the drier foodstuff unaffected or slightly warm.

But in the non-thermal APPD, the main reason for this positive relationship could be due to the increase in the chemical species, including ROS noted for their catalytic activity and biological significance, highly energetic electrons, electromagnetic radiation, and thermal effects, which individually and synergistically affect the treated target (Lu et al., Reference Lu, Laroussi and Puech2012; Bazaka et al., Reference Bazaka, Jacob and Ostrikov2015). These effects have been exploited to induce stress, thus may stimulate the death that occurred in larvae and adults due to oxidative stress of plasma in this work. Exposure to plasma may damage the cuticle and epidermis and produce damage signals to attract hemocytes to the affected area. This might cause further clotting and melanization which is a defensive response trying to heal the damage due to ROS by the disintegration of fat bodies. Similar responses were found in Drosophila melanogaster larva by Ferreira et al. (Reference Ferreira, Gomes, Benilov and Khadem2016).

One hundred percent mortality was achieved for T. castaneum larvae and T. granarium adults at 5.4 W for an exposure time of 120 and 90 s to non-thermal APPD, respectively. While complete (100%) mortality was achieved for T. castaneum adults and larvae at 300 and 180 W for an exposure time of 90 and 150 s to the microwave power, respectively. Whereas for T. granarium adults and larvae 100% mortality was achieved at 180 and 300 W for an exposure time of 120 and 150 sec to the microwave power, respectively; a similar observation was found by Vadivambal et al. (Reference Vadivambal, Deji, Jayas and White2010) who evaluated the potential of microwave radiation to eliminate larval and adult stages of T. castaneum at 600 W for an exposure time of 14 s. The results are to some extent consistent with that reported by Ahmady et al. (Reference Ahmady, Mousa and Zaitoun2016), who studied the microwave radiation effect on T. confusum and Callosobruchus maculatus at 400 W and found that complete mortality of T. confusum adults was obtained at 25 s, whereas 98.8% mortality percentage was obtained at the same exposure time for C. maculatus adults. Zinhoum et al. (Reference Zinhoum, Negm, Abd-El Hameed and Afify2019) stated that adult mortality of Stegobium paniceum increased by increasing the exposure time at different exposure powers of microwave (low, medium, and high). The mortality of pulse beetle was found to increase with the increase in microwave exposure time and power level or both (Singh et al., Reference Singh, Singh and Kotwaliwale2012).

The effect of non-thermal APPD was studied against insects by Mishenko et al. (Reference Mishenko, Malinin, Rashkovan, Basteev, Bazyma, Mazalov and Kutovoy2000). They found that treating S. granarius using a combination of radiation and plasma discharge resulted in 100% mortality. Keever et al. (Reference Keever, Dowdy, Bures, Hankins and Bourham2001) used a helium-based non-thermal APPD to treat Lasioderma serricorne. They found that a 70 s exposure to the non-thermal APPD resulted in 92% mortality of adults 2 days after treatment. By changing some variables, such as time, the insecticidal effect of plasma can be changed. In accordance with Donohue et al. (Reference Donohue, Bures, Bourham and Roe2006), our results showed that the major influence on the mortality for both pests was achieved with exposure time and different power levels 24 h post-exposure to non-thermal APPD and microwave energy. On the other hand, the exposure time had the foremost effect on the mortality for both pests at different power levels 7 days post-exposure to non-thermal APPD with no effect of the applied power. While both factors (time and power level) had the foremost effect on the mortality percent of T. castaneum and T. granarium adults and larvae post-exposure to microwave energy. Microwave heating can effectively eliminate insects of all life stages (egg, young larva, old larva, pupa, and adult) from stored grains at the optimum microwave power and LT (Vadivambal et al., Reference Vadivambal, Jayas and White2008; Purohita et al., Reference Purohita, Jayasa, Yadav, Chelladuraia, Fields and White2013).

The expected exposure time to cause 50 and 90% mortality values decreased with increased exposure time and power level for both insects after 24 h and 7 days post-exposure to non-thermal APPD and microwave energy. It was found that microwave was more effective after 24 h, while non-thermal APPD plasma was more effective after 7 days. The smaller the LT50 and LT90 the better, so the time needed to kill the T. castaneum and T. granarium adults and larvae is decreased, so the time efficiency was achieved. These findings are in harmony with that of Zinhoum et al. (Reference Zinhoum, Negm, Abd-El Hameed and Afify2019). Trogoderma granarium larvae were the most tolerant life stage to both non-thermal APPD and microwave energy. The expected exposure time to cause 90% mortality values for T. granarium larvae was greater than those for the adult stage of the same insect and greater than those of T. castaneum adults and larvae at the same power levels after 7 days of exposure to non-thermal APPD and microwave energy. While T. granarium adults and T. castaneum larvae were the most susceptible to both non-thermal APPD and microwave powers. Increases in time had the intense effect of increasing susceptibility of all life stages and species. A decrease in the exposure time was estimated to achieve target levels of mortality in nearly all cases with each increase in power levels. One explanation is that the presence of long dense larval hairs reduces the direct body exposed to the non-thermal APPD and microwave energy. In addition, the presence of the food source provided when larvae are exposed to the non-thermal APPD and microwave powers may have helped to reduce larval exposure or provided a means for larvae to limit or escape exposure (Toews et al., Reference Toews, Campbell and Arthur2010; Kharel et al., Reference Kharel, Arthur, Zhu, Campbell and Subramanyam2014). Trogoderma granarium adults were generally more susceptible than larvae. However, the greater mortality obtained for adults could be due to the absence of long dense hairs similar to larvae. These results agree with those obtained in a recent study using three species of T. granarium. Results show consistently that adults are more susceptible to insecticides compared to larvae (Athanassiou et al., Reference Athanassiou, Kavallieratos, Boukouvala, Mavroforos and Kontodimas2015; Ghimire et al., Reference Ghimire, Arthur, Myers and Phillips2016).

Reactive species such as hydrogen peroxide and nitric oxide are known to have effects on many developmental processes in plants (Domingos et al., Reference Domingos, Prado, Wong, Gehring and Feijo2015; Mittler, Reference Mittler2017). The oxidative stress of plasma effects has been exploited to induce stress and thus selectively stimulate seed germination (Ji et al., Reference Ji, Choi, Pengkit, Im, Kim, Kim, Park, Hong, Jung, Choi and Park2016; Zhou et al., Reference Zhou, Zhou, Zhang, Zhuang, Yang, Bazaka and Ostrikov2016). Generally, our results revealed that wheat grains viability (in terms of wheat germination) was increased by increasing the time of non-thermal APPD application. Exposure time to cause 50% mortality significantly decreased post-exposure to non-thermal APPD compared to exposure time to cause 90% mortality. These data indicated that non-thermal APPD at this time did not harm the wheat grains, i.e. normal texture, color and appearance, germination percent only were influenced. Germination of wheat grains treated with LT90's levels of non-thermal APPD showed that the plasma grain treatment for an appropriate time that ranged from 1.9 to 3.1 min (112.55–182.97 sec) improved the germination. Germination acceleration is further enhanced with an increase of exposition time from 11% for 3 min plasma treatment to around 40% for 30 min plasma treatment of germinated wheat grains (Nishime et al., Reference Nishime, Wannicke, Horn, Weltmann and Brust2020). A similar result was found in the study of Los et al., (Reference Los, Ziuzina, Akkermans, Boehm, Cullen, Van Impe and Bourke2018); short plasma treatment had a minimal positive influence on the germination rate of wheat. In the experiment described in Ziuzina et al. (Reference Ziuzina, Los, Akkermans, Boehm, Cullen, Van Impe and Bourke2018), the grain germination percentage of samples treated for up to 5 min was not affected, but it was decreased after 20 min of non-thermal plasma treatment. Our results go in line with those of Jiafeng et al. (Reference Jiafeng, Xin, Ling, Jiangang, Hanliang, Qilai, Renhong and Yuanhua2014) who mentioned a significant increase in the germination potential of wheat grains post-exposure by cold plasma. Also, as reported in the available study, using DBD plasma with various surrounding gases (oxygen, air, argon, and nitrogen), they observed a significant increase of germination potential by 24.0, 28.0, and 35.5% after 4 min of exposure (Meng et al., Reference Meng, Qu, Wang, Sun, Liang and Hu2017). Li et al. (Reference Li, Wang, Meng, Qu, Sun, Liang and Hu2017) reported that wheat grains germination increased after 7 min of non-thermal plasma treatment. Gidea et al. (Reference Gidea, Magureanu, Teodorescu, Iosub and Cimpoceriu2017) showed that the plasma grain treatment for an appropriate time improved the germination rate, speed of germination, and speed of growth in the early stage. The same authors also presented the hypothesis that the changes in the wheat grain germination characteristics suggested an appropriate DBD plasma treatment dose to promote wheat grain germination. Also, the grains treated for 3 and 6 min had the highest germination rate of 95–100% (Roy et al., Reference Roy, Hasan, Kabir, Reza, Talukder and Chowdhury2018a). However, further increments of non-thermal plasma treatment time caused a non-significant decrease in the germination rate. Similarly, Roy et al. (Reference Roy, Hasan, Talukder, Hossain and Chowdhury2018b) reported that germination rate, germination index, and vigor index increased for all used exposition times and atmospheres, with an optimal exposure time of 6–9 min. Los et al. (Reference Los, Ziuzina, Akkermans, Boehm, Cullen, Van Impe and Bourke2018) stated that short plasma treatment had minimal influence on the germination rate of wheat; however, extending treatment time up to 20 min negatively affected this qualitative parameter. In the experiment described in Ziuzina et al. (Reference Ziuzina, Los, Akkermans, Boehm, Cullen, Van Impe and Bourke2018), the grain germination percentage of samples treated for up to 5 min was not affected, but it was decreased after 20 min of non-thermal plasma treatment. In conclusion, the enhancement of the wheat seed germination depends on the cold plasma dose; the dose value of RONS can play an essential role in the control of growth and improvement of plants (Matra, Reference Matra2016).

Microwave radiation is often broadly classified and induces thermal and non-thermal effects in the biological system of plant seeds which depends mainly on power (Lazim and Ramadhan, Reference Lazim and Ramadhan2020). A significant decrease (P < 0.05) in wheat grain germination was observed after treatment with microwave energy at a power level of 300 W at LT50. The negative effect of all microwave treatments on germination percent increased with increasing exposure time (LT90). A shorter exposure time (10.8 s) showed a stimulating effect than the longer one. These results are in line with Wang et al., (Reference Wang, Wang and Guo2018) who found that the best germination percentage appeared when exposing the wheat grains for 10 s to microwave radiation. Similar results have been reported for bean (Tomasz, Reference Tomasz2015) and pepper seeds (Matwijczuk et al., Reference Matwijczuk, Kornarzyñski and Pietruszewski2012). While the longer exposure time (LT90) of microwave radiation treatment of wheat grains had an inhibitory effect on germination percent. These results are in resemblance to the research evidence obtained by Aladjadjiyan (Reference Aladjadjiyan2010) who study the influence of microwave irradiation treatment with the frequency of 2.45 GHz on the germination of lentil seeds that ascertained that longer exposure time had an inhibitory effect on plant development as well as the higher output power of microwave irradiation. The increase in the microwave seed exposure level to microwave showed a significant negative effect on seed germination (Lazim and Ramadhan, Reference Lazim and Ramadhan2020). Similar results for corn seed have been reported by Ashabahebwa et al. (Reference Ashabahebwa, Wang-Hee and ByoungKwan2015). Further increase in the exposure time and power level leads to increasing rate and extent of physical damage and thus leads to hard negative results (Kuzugudenli, Reference Kuzugudenli2018). Also, the vibration of water molecule dipoles induced by microwave radiation is another effect of microwave on water molecules within the seed plant that give a thermal effect that affects the reaction rate in biological processes according to van Hoff's rule and Arrhenius, the law affects reaction rate in biological processes. Some studies have shown positive and negative impacts of microwave on the germination of wheat grain cultivars (Nikulin et al., Reference Nikulin, Kovalev and Chang2009; Lakshmappa et al., Reference Lakshmappa, Seema, Ramachandran and Manmohan2011; Abdelghafar, Reference Abdelghafar2015). The present research revealed that there is a significant increase (P < 0.05) in the activity of CAT in the larvae of both insects and adults of T. granarium and also no significant difference (P > 0.05) among T. castaneum adults compared to that in the control. Consequently, the increase in CAT activity after the treatment of adults and larvae with non-thermal APPD could be expected in order to scavenge hydrogen peroxide. CAT is one of the most potent catalysts known. This enzyme catalyzes the dismutation of two molecules of H2O2, a powerful and potentially harmful oxidizing agent, to water and molecular oxygen (Karra et al., Reference Karra, Pulvin, Meziani, Thomas, Touraud and Kunz2003). Several researchers have found similar results for the activity of CAT in insect bodies under different stress conditions (Krishnan and Kodrík, Reference Krishnan and Kodrík2006; Fahmy, Reference Fahmy2012; Madhusudhan et al., Reference Madhusudhan, Iresh-Kumar, Singh, Sinha, Kirankumar and Prasad2012). In consistence with our results, Abd El-Aziz et al. (Reference Abd El-Aziz, Mahmoud and Elaragi2014) reported that there was a significant change (P < 0.05) in the enzymes of the antioxidant defense system to maintain homeostasis in P. interpunctella after atmospheric pressure plasma jet treatment as a result of the oxidative stress due to radicals.

Also, part of the system is GST which catalyzes the conjugation of glutathione reductase to nucleophilic xenobiotics or cellular components damaged by oxyradical attack resulting in their detoxification (Vontas et al., Reference Vontas, Small and Hemingway2001; Fahmy Reference Fahmy2012) that proved that GST is involved in the inactivation of toxic lipid peroxidation products accumulated during destructive processes caused by two insect growth regulators which enhance the oxidative stress and antioxidant efficiency of the cotton leafworm, Spodoptera littoralis.

Peroxidases provide one of the protective mechanisms in the cell against any harmful effects of free radicals (Iiyama et al., Reference Iiyama, Chieda, Lee, Kusakabe, Yasunaga-Aoki and Shimizu2007). Peroxidases are antioxidants and have a significant role in the regulation of cell life, proliferation, and death. It prevents damage to important cellular components caused by ROS. It has been involved in cell protection from the noxious effect of excess oxidant stress (Pompella et al., Reference Pompella, Athanase, Aldo, Vincenzo De and Alessandro2003). According to our results, peroxidases play an important role in protecting cells in all stages in both insects against the antioxidant effect of non-thermal APPD application, as a significant decrease in the level of its activity was observed in treatment compared to control after 24 h. The lower titer of peroxidases in this study may be due to its consumption in scavenging the generated ROS. Similar results were mentioned in Bacillus thuringiensis-treated Aedes caspius larvae where B. thuringiensis inhibited induction of the anti-stress factor, peroxidases, and hence larvae died within 24 h of treatment (Ahmed, Reference Ahmed2011). The depletion of peroxidases because of oxidative stress is another possible reason for the observed rise in the peroxidase level in the tissues of organisms (Vijayavel and Balasubramanian, Reference Vijayavel and Balasubramanian2009). Our result agrees with the finding of Pankaj et al. (Reference Pankaj, Misra and Cullen2013) who reported that cold plasma has been reported to inactivate a range of enzymes such as polyphenol oxidase and peroxidase.

The results revealed in this study indicated the potential of these enzymes considered as an indicative criterion to the degree of damaged occurred in T. castaneum and T. granarium after 24 h of non-thermal APPD application. These results go with that of Brown et al. (Reference Brown, Cook, Lipton and Coleman2012) who concluded that LDH is an enzyme that is expressed at high levels when the cell is exposed to stress and/or damaged. Also, LDH is used as an indicative criterion of exposure to chemical stress or toxic materials (Wu and Lam, Reference Wu and Lam1997; Nathan et al., Reference Nathan, Kalaivani, Chung and Murugan2006). The LDH is a parameter that is widely used in toxicology and clinical chemistry to diagnose cell, tissue, and organ damage (Ribeiro et al., Reference Ribeiro, Guilhermino, Sousa and Soares1999). The current results of disturbed LDH activity in T. castaneum and T. granarium by non-thermal APPD application indicate that this technique of the treatment might be affecting the synthesis or functional levels of LDH, directly or indirectly by altering the cytomorphology of the cells. Also, the induction or inhibition of the LDH activities as recorded in the present study might be on molecular levels, referred to as depression or mutations of the regulating genes responsible for the biosynthesis of polypeptide chains building this enzyme (Bencheraiet et al., Reference Bencheraiet, Kherrab, Kabouche, Kabouche and Maurice2011; Bhandary et al., Reference Bhandary, Kumari, Bhat, Sharmila and Bekal2012). Also, Qari et al. (Reference Qari, Abdel-Fattah and Shehawy2017) reported that LDH activity has been disturbed by plant extracts and insecticides as reported in the available study.

Differently, the total protein levels were insignificantly decreased in T. granarium adults and larvae compared to control. Free radicals can adversely alter proteins and can result in loss of enzyme activity (Devasagayam et al., Reference Devasagayam, Tilak, Boloor, Sane, Ghaskadbi and Lele2004). The consequences of protein damage as a response mechanism to oxidative stress are loss of enzymatic activity, altered cellular functions such as energy production, interference with the creation of membrane potentials, and changes in the type and level of cellular proteins (Grune, Reference Grune2020). Proteins are major targets for radicals and two-electron oxidants in biological systems due to their abundance and high-rate constants for reaction (Michael, Reference Michael2016). Consequently, increased oxidative stress leads to enhanced regulation of antioxidants and these processes had been mirrored in insect physiological adaptations and resistance. Once inside the cell, ROS can induce significant damage (P < 0.05) to intracellular components of the organism, including carbohydrates, lipids, proteins, and nucleic acids, affecting cellular metabolism, and, at sufficiently high concentration, leading to cell death (Jukapli and Bagheri, Reference Jukapli and Bagheri2016; Tallósy et al., Reference Tallósy, Janovák, Nagy, Deák, Juhász, Csapó, Buzás and Dékány2016).

Conclusion

Current technologies involve the use of non-chemical processes that are effective in disinfesting insect pests in stored grains. However, they come with their specific own set of challenges, based on the results of microwave disinfestation, it is considered a safe method to other quarantine methods and can avoid problems of food safety and environmental pollution. Complete mortality, that is, 100% could be achieved using microwave energy in a short time. Although microwaves have the potential for disinfecting the food products, they have not been used widely because there are no industrial installations that can treat deep in the grain bulk. It is possible to use microwave energy on thin layers on belts but not in bulk. The microwave technology needs to be further developed to meet industry needs and provide economically feasible installations that can compete with existing storage insect control technologies.

Non-thermal plasma is a recently proposed emerging field and one potential topic is pest control in stored products. The plasma generated at atmospheric pressure should be further investigated as an alternative non-toxic pest control method to control pests in stored products as it does not leave any chemical residue on the treated food products. Further studies are required in the design and development of commercial and continuous cold plasma treatment and what the economic, ecological, and consumer benefits and acceptability are.

Acknowledgements

We are grateful to Prof. Dr Mohamed Abou Seta who is responsible for Statistical Department Lab., Plant Protection Research Institute, Agricultural Research Center, Dokki, Giza, Egypt for aiding in statistical analysis and advice on data handling, and we benefited from helpful conversations with him.

References

Abbott, WS (1925) A method of computing the effectiveness of an insecticide. Journal of Entomology 18, 265267.Google Scholar
Abd El-Aziz, MF, Mahmoud, EA and Elaragi, GM (2014) Non thermal plasma for control of the Indian meal moth, Plodia interpunctella (Lepidoptera: Pyralidae). Journal of Stored Products Research 59, 215221.CrossRefGoogle Scholar
Abd El-Raheem, AM and Said, SM (2016) Does microwave radiation have an effect on stored product insects and their host food quality? Academic Journal of Entomology 9, 5161.Google Scholar
Abdelghafar, AE (2015) Effect of microwave electromagnetic radio frequency on germination and seedling growth consequences of six wheat Triticum aestivum L. cultivars. Advances in Environmental Biology 9, 270280.Google Scholar
Aebi, H (1984) Catalase in vitro. Methods in Enzymology 105, p121.CrossRefGoogle ScholarPubMed
Ahmady, A, Mousa, MA and Zaitoun, AA (2016) Effect of microwave radiation on Tribolium confusum Jaquelin du Val (Coleoptera: Tenebrionidae) and Callosobruchus maculatus (F.) (Coleoptera: Chrysomelidae: Bruchidae). Journal of Entomology and Zoology Studies 4, 12571263.Google Scholar
Ahmed, AM (2011) Immune and antioxidant defenses in an autogenous Aedes caspius mosquito upon infection with Bacillus thuringiensis Kurstaki. African Journal of Microbiology Research 5, 38483857.Google Scholar
Ahmedani, MS, Haque, MI, Afzal, SN, Aslam, M and Naz, S (2009) Varietal changes in nutritional composition of wheat kernel (Triticum aestivum L.) caused by khapra beetle infestation. Pakistan Journal of Botany 41, 15111519.Google Scholar
Aladjadjiyan, A (2010) Effect of microwave irradiation on seeds of lentils (Lens culinaris Med. Romanian Journal of Biophysics 20, 213221.Google Scholar
Anonymous (2003) SAS Statistics and graphics guide, release 9.1. SAS Institute, Cary, North Carolina 27513, USA.Google Scholar
Ashabahebwa, A, Wang-Hee, LC and ByoungKwan, C (2015) Effect of microwave heat treatment on inhibition of corn seed germination. Journal of Biosystems Engineering 40, 224231.Google Scholar
Athanassiou, CG, Kavallieratos, NG, Boukouvala, MC, Mavroforos, ME and Kontodimas, DC (2015) Efficacy of alpha-cypermethrin and thiamethoxam against Trogoderma granarium Everts (Coleoptera: Dermestidae) and Tenebrio molitor L. (Coleoptera: Tenebrionidae) on concrete. Journal of Stored Products Research 62, 101107.CrossRefGoogle Scholar
Bazaka, K, Jacob, MV and Ostrikov, K (2015) Sustainable life cycles of natural-precursor-derived nanocarbons. Chemical Reviews 116, 163214.CrossRefGoogle ScholarPubMed
Bencheraiet, R, Kherrab, H, Kabouche, A, Kabouche, Z and Maurice, J (2011) Flavonols and antioxidant activity of Ammi visnaga L. (Apiaceae). Records of Natural Products 5, 5255.Google Scholar
Benhalima, H, Chaudhry, MQ, Mills, KA and Price, NR (2004) Phosphine resistance in stored-product insects collected from various grain storage facilities in Morocco. Journal of Stored Products Research 40, 241249.CrossRefGoogle Scholar
Bhandary, SK, Kumari, SN, Bhat, VS, Sharmila, KP and Bekal, MP (2012) Preliminary phytochemical screening of various extracts of Punica granatum peel, whole fruit and seeds. Journal of Health Sciences 2, 3438.Google Scholar
Bhattacharya, M and Basak, T (2017) A comprehensive analysis on the effect of shape on the microwave heating dynamics of food materials. Innovative Food Science & Emerging Technologies 39, 247266.CrossRefGoogle Scholar
Bhesh, BT and Raju, BT (2019) Study of dielectric barrier discharge in air and estimation of electron density and energy deposition. Journal of Science and Engineering 7, 19.Google Scholar
Bradford, MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of proteins utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248254.CrossRefGoogle ScholarPubMed
Brown, JE, Cook, RJ, Lipton, J and Coleman, RE (2012) Serum lactate dehydrogenase is prognostic for survival in patients with bone metastases from breast cancer: a retrospective analysis in bisphosphonate-treated patients. Clinical Cancer Research 18, 63486355.CrossRefGoogle ScholarPubMed
Carpen, LG, Chireceanu, C, Teodorescu, M, Chiriloaie, A, Teodoru, A and Dinescu, G (2019) The effect of argon/oxygen and argon/nitrogen atmospheric plasma jet on stored products pests. Romanian Journal of Physics 64, 503.Google Scholar
Chen, Q, Chen, X, Chen, ZZ, Zhang, B and Zheng, YQ (2019) High-efficiency microwave heating method based on impedance matching technology. AIP Advances 9, 015113.CrossRefGoogle Scholar
Devasagayam, TPA, Tilak, JC, Boloor, KK, Sane, KS, Ghaskadbi, SS and Lele, RD (2004) Free radicals and antioxidants in human health current status and future prospects. Journal of Association of Physicians of India 52, 794804.Google ScholarPubMed
DGCK (1972) Deutsche Gesellschaft für Klinische chemie (1972). Empfehlungender Deutschen Gessellschaft für Klinische chemie (DGCK). Journal of Clinical Chemistry and Clinical Biochemistry 10, 182193.Google Scholar
Domingos, P, Prado, AM, Wong, A, Gehring, C and Feijo, JA (2015) Nitric oxide: a multitasked signaling gas in plants. Molecular Plant 8, 506520.CrossRefGoogle ScholarPubMed
Domingue, MJ, Morrison, WR, Yeater, K and Myers, S (2020) Oleic acid emitted from frozen Trogoderma spp. larvae causes behavioral aversion. Chemoecology 30, 161172.CrossRefGoogle Scholar
Donohue, KV, Bures, BL, Bourham, MA and Roe, RM (2006) Mode of action of a novel nonchemical method of insect control: atmospheric pressure plasma discharge. Journal of Economic Entomology 99, 3847.CrossRefGoogle ScholarPubMed
Fahmy, NM (2012) Impact of two insect growth regulators on the enhancement of oxidative stress and antioxidant efficiency of the cotton leafworm, Spodoptera littoralis (Biosd.). Egyptian Academic Journal of Biological Sciences 5, 137149.CrossRefGoogle Scholar
FAO (2008) ‘Insect damage: damage on post-harvest’ (PDF). In Compendium on Post-harvest Operations.Google Scholar
Ferreira, MI, Gomes, JGL, Benilov, MS and Khadem, M (2016) Effects of nonthermal atmospheric-pressure plasma on Drosophila development. Plasma Medical 6, 115124.CrossRefGoogle Scholar
Ghimire, MN, Arthur, FH, Myers, SW and Phillips, TW (2016) Residual efficacy of deltamethrin and β-cyfluthrin against Trogoderma variabile and Trogoderma inclusum (Coleoptera: Dermestidae). Journal of Stored Products Research 66, 611.CrossRefGoogle Scholar
Gidea, M, Magureanu, M, Teodorescu, R, Iosub, L and Cimpoceriu, D (2017) The impact of plasma treatment over wheat seeds. Proceedings of the 17th International Multidisciplinary Scientific Geo Conference SGEM Conference, pp. 361–368, Albena, Bulgaria.CrossRefGoogle Scholar
Grune, T (2020) Oxidized protein aggregates: formation and biological effects, free radical biology and medicine, 10.1016/. Journal of Free Radical Biology and Medicine 150, 120124.CrossRefGoogle Scholar
Habig, WH, Pabst, MJ and Jakoby, WB (I974) Glutathione S-transferase. The first enzymatic step in mercapturic acid formation. Journal of Biological Chemistry 249, 71307139.CrossRefGoogle Scholar
Hammerschmidt, R, Nuckles, F and Kuc, J (1982) Association of enhanced peroxidase activity with induced systemic resistance of cucumber to Colletotrchum lagenarium. Physiological Plant Pathology 20, 7382.CrossRefGoogle Scholar
Iiyama, K, Chieda, Y, Lee, JM, Kusakabe, T, Yasunaga-Aoki, C and Shimizu, S (2007) Effect of superoxide dismutase gene inactivation on virulence of Pseudomonas aeruginosa PAO1 toward the silkworm, Bombyx mori. Applied and Environmental Microbiology 73, 15691575.CrossRefGoogle ScholarPubMed
Ishaaya, I (1971) Observations on the phenoloxidase system in the armored scales Aonidiella aurantii and Chrysomphalus aonidum. Comparative Biochemistry & Physiology 39, 935943.Google ScholarPubMed
Ji, SH, Choi, KH, Pengkit, A, Im, JS, Kim, JS, Kim, YH, Park, Y, Hong, EJ, Jung, SK, Choi, EH and Park, G (2016) Effects of high voltage nanosecond pulsed plasma and micro DBD plasma on seed germination, growth development and physiological activities in spinach. Archives of Biochemistry and Biophysics 605, 117128.CrossRefGoogle ScholarPubMed
Jiafeng, J, Xin, H, Ling, LI, Jiangang, L, Hanliang, S, Qilai, X, Renhong, Y and Yuanhua, D (2014) Effect of cold plasma treatment on seed germination and growth of wheat. Plasma Science and Technology 16, 5458.Google Scholar
Jukapli, NM and Bagheri, S (2016) Recent developments on Titania nanoparticle as photocatalytic cancer cells treatment. Journal of Photochemistry and Photobiology B 163, 421430.CrossRefGoogle ScholarPubMed
Karabulut, OA and Baykal, N (2002) Evaluation of the use of microwave power for the control of postharvest diseases of peaches. Postharvest Biology and Technology 26, 237240.CrossRefGoogle Scholar
Karra, CM, Pulvin, S, Meziani, A, Thomas, D, Touraud, D and Kunz, W (2003) Bio-oxidation of n-hexanol by alcohol oxidase and catalase in biphasic and micellar systems without solvent. Biotechnology & Bioengineering 81, 2732.Google Scholar
Keever, D, Dowdy, AK, Bures, BL, Hankins, OE and Bourham, MA (2001) Mortality and sterility of the cigarette beetle, Lasioderma serricorne (F.), due to exposure to atmospheric plasma. 2001 Annual Research Conference on Methyl Bromide Alternatives and Emissions Reductions. San Diego, California, 128, 1–4.Google Scholar
Kharel, K, Arthur, FH, Zhu, KY, Campbell, JF and Subramanyam, B (2014) Susceptibility of different life stages of Tribolium confusum to pyrethrin aerosol: effects of a flour food source on insecticidal efficacy. Journal of Pest Science 87, 295300.CrossRefGoogle Scholar
Kim, B, Yun, H, Jung, S, Jung, Y, Jung, H, Choe, W and Jo, C (2011) Effect of atmospheric pressure plasma on inactivation of pathogens inoculated onto bacon using two different gas compositions. Food Microbiology 28, 913.CrossRefGoogle ScholarPubMed
Konradsen, F, Van Der Hoek, W, Cole, DC, Hutchinson, G, Daisley, H, Singh, S and Eddleston, M (2003) Reducing acute poisoning in developing countries options for restricting the availability of pesticides. Toxicology 192, 249261.CrossRefGoogle ScholarPubMed
Kostov, KG, Nishime, TMC, Hein, LRO and Toth, A (2013) Study of polypropylene surface modification by air dielectric barrier discharge operated at two different frequencies. Surface & Coatings Technology 234, 6066.CrossRefGoogle Scholar
Krishnan, N and Kodrík, D (2006) Antioxidant enzymes in Spodoptera littoralis (Boisduval): are they enhanced to protect gut tissues during oxidative stress? Journal of Insect Physiology 52, 1120.CrossRefGoogle ScholarPubMed
Kumar, S, Mohapatra, D, Kotwaliwale, N and Singh, KK (2016) Vacuum hermetic fumigation for food grains storage. pp. 252–255. Navarro S, Jayas DS, Alagusundaram K (Eds.) Proceedings of the 10th International Conference on Controlled Atmosphere and Fumigation in Stored Products (CAF2016), CAF Permanent Committee Secretariat, Winnipeg, Canada.Google Scholar
Kuzugudenli, E (2018) Effect of microwave radiation on growth and germination of stone pine (Pinus pinea L.) seedlings. Applied Ecology and Environmental Research 16, 28372844.CrossRefGoogle Scholar
Lakshmappa, R, Seema, M, Ramachandran, V and Manmohan, SB (2011) Effects of low-power microwave fields on seed germination and growth rate. Journal of Electromagnetic Analysis and Applications 3, 165171.Google Scholar
Lazim, SK and Ramadhan, M (2020) Study effect of a static magnetic field and microwave irradiation on wheat seed germination using different curves fitting model. Journal of Green Engineering 10, 31883205.Google Scholar
Li, J, Lehmann, S, Weißbecker, B, Ojeda Naharros, I, Schütz, S, Joop, G and Wimmer, EA (2013) Odoriferous defensive stink gland transcriptome to identify novel genes necessary for quinone synthesis in the red flour beetle, Tribolium castaneum. PLoS Genetics 9, e1003596.CrossRefGoogle ScholarPubMed
Li, Y, Wang, T, Meng, Y, Qu, G, Sun, Q, Liang, D and Hu, S (2017) Air atmospheric dielectric barrier discharge plasma induced germination and growth enhancement of wheat seed. Plasma Chemistry and Plasma Processing 37, 16211634.CrossRefGoogle Scholar
Los, A, Ziuzina, D, Akkermans, S, Boehm, D, Cullen, PJ, Van Impe, J and Bourke, P (2018) Improving microbiological safety and quality characteristics of wheat and barley by high voltage atmospheric cold plasma closed processing. Food Research International 106, 509521.CrossRefGoogle ScholarPubMed
Lowe, S, Browne, M, Boudjelas, S and de Poorter, M (2000) 100 of the World's Worst Invasive Alien Species: A Selection From the Global Invasive species Database. New Zealand: Invasive Species Specialist Group, World Conservation Union (IUCN), 2000.Google Scholar
Lu, X, Laroussi, M and Puech, V (2012) On atmospheric-pressure non equilibrium plasma jets and plasma bullets. Plasma Sources Science Technology 21, 034005.CrossRefGoogle Scholar
Madhusudhan, KN, Iresh-Kumar, N-DC, Singh, GP, Sinha, AK, Kirankumar, KP and Prasad, BC (2012) Impact of pebrine infection on catalase activity in tropical tasar silkworm (Antheraea mylitta D). International Journal of Science and Nature 3, 212213.Google Scholar
Manickavasagan, A, Alahakoon, PMK, Al-Busaidi, TK, Al-Adawi, S, Al-Wahaibi, AK, Al-Raeesi, AAJayas, DS (2013) Disinfestation of stored dates using microwave energy. Journal of Stored Products Research 55, 15.CrossRefGoogle Scholar
Matra, K (2016) Non-thermal plasma germination enhancement of radish seeds. Procedia Computer Science 86, 132135.CrossRefGoogle Scholar
Matwijczuk, A, Kornarzyñski, K and Pietruszewski, S (2012) Effect of magnetic field on seed germination and seedling growth of sunflower. International Agrophysics 26, 271278.CrossRefGoogle Scholar
Meng, Y, Qu, G, Wang, T, Sun, Q, Liang, D and Hu, S (2017) Enhancement of germination and seedling growth of wheat seed using dielectric barrier discharge plasma with various gas sources. Plasma Chemistry and Plasma Processing 37, 11051119.CrossRefGoogle Scholar
Michael, JD (2016) Protein oxidation and peroxidation. Biochemical Journal 473, 805825.Google Scholar
Mishenko, AA, Malinin, OAV, Rashkovan, M, Basteev, AV, Bazyma, LA, Mazalov, YP and Kutovoy, VA (2000) Complex high-frequency technology for protection of grain against pests. Journal of Microwave Power and Electromagnetic Energy 35, 179184.CrossRefGoogle ScholarPubMed
Mittler, R (2017) ROS are good. Trends in Plant Science 22, 1119.CrossRefGoogle ScholarPubMed
Mohammadi, S, Imani, S, Dorranian, D, Tirgari, S and Shojaee, M (2015) The effect of non-thermal plasma to control of stored product pests and changes in some characters of wheat materials. Food Engineering Reviews 7, 150156.Google Scholar
Myers, SW and Hagstrum, DH (2012) Quarantine in stored product protection. In Hagstrum, DH, Philips, TW and Cuperus, G (eds), Manhattan, KS: Kansas State Univ, 297304.Google Scholar
Nasr, MEH, Zinhoum, RA and Lotfy, K (2020) Efficacy of cold plasma against three of stored grain insects. International Journal of Entomology Research 5, 115117.Google Scholar
Nathan, SS, Kalaivani, K, Chung, KG and Murugan, K (2006) Effect of neem limonoids on lactate dehydrogenase (LDH) of the rice leaf folder, Cnaphalocrocis medinalis (Guenee) (Insecta: Lepidoptera: Pyralidae). Chemosphere 62, 13881393.CrossRefGoogle Scholar
Nikulin, RN, Kovalev, IA and Chang, LH (2009) The effect of low-intensity microwave radiation on germinating and growth intensity of wheat grains. 19th International Crimean Conference Microwave and Telecommunication Technology. Sevastopol, Russia, p. 887–888.Google Scholar
Nishime, T, Wannicke, N, Horn, S, Weltmann, KD and Brust, H (2020) A coaxial dielectric barrier discharge reactor for treatment of winter wheat seeds. Applied Sciences 10, 7133.CrossRefGoogle Scholar
Özberk, F (2018) Impacts of khapra beetle (T. granarium Everts) onto marketing price and relevant traits in bread wheat (T. aestivum L. Applied Ecology and Environmental Research 16, 61436153.CrossRefGoogle Scholar
Pankaj, SK, Misra, NN and Cullen, PJ (2013) Kinetics of tomato peroxidase inactivation by atmospheric pressure cold plasma based on dielectric barrier discharge. Innovative Food Science & Emerging Technologies 19, 153157.CrossRefGoogle Scholar
Pompella, A, Athanase, V, Aldo, P, Vincenzo De, T and Alessandro, FC (2003) The changing faces of glutathione, a cellular protagonist. Biochemical Pharmacology 66, 14991503.CrossRefGoogle ScholarPubMed
Pranavi, S, Prasad, MSK and Lakshmipathi, V (2016) Complete study of the life cycle of Tribolium castaneum and its weight variations in the developing stages. International Journal of Plant, Animal and Environmental Sciences 6, 95100.Google Scholar
Purohita, P, Jayasa, DS, Yadav, BK, Chelladuraia, V, Fields, PG and White, NDG (2013) Microwaves to control Callosobruchus maculatus in stored mung bean (Vigna radiata). Journal of Stored Products Research 53, 1922.CrossRefGoogle Scholar
Qari, SH, Abdel-Fattah, NAH and Shehawy, AA (2017) Assessment of DNA damage and biochemical responses in Rhyzopertha dominica exposed to some plant volatile oils. Journal of Pharmacology and Toxicology 12, 8796.CrossRefGoogle Scholar
Ribeiro, S, Guilhermino, L, Sousa, JP and Soares, AMVM (1999) Novel bioassay based on acetylcholinesterase and lactate dehydrogenase activities to evaluate the toxicity of chemicals to soil isopods. Ecotoxicology and Environmental Safety 44, 287293.CrossRefGoogle ScholarPubMed
Roy, NC, Hasan, MM, Kabir, AH, Reza, MA, Talukder, MR and Chowdhury, AN (2018a) Atmospheric pressure gliding arc discharge plasma treatments for improving germination, growth and yield of wheat. Plasma Science and Technology 20, 115501.CrossRefGoogle Scholar
Roy, NC, Hasan, MM, Talukder, MR, Hossain, MD and Chowdhury, AN (2018b) Prospective applications of low frequency glow discharge plasmas on enhanced germination, growth and yield of wheat. Plasma Chemistry and Plasma Processing 38, 1328.CrossRefGoogle Scholar
Rustamani, MA, Khatri, I, Sultana, R and Laghari, MH (2014) Population fluctuation of red flour beetle, Tribolium castaneum (Herbst.) (Coleoptera: Tenebrionidae) on different cereal foods in laboratory. Pakistan Journal of Zoology 46, 15111514.Google Scholar
Singh, R, Singh, KK and Kotwaliwale, N (2012) Study on disinfestation of pulses using microwave technique. Journal of Food Science and Technology 49, 505509.CrossRefGoogle Scholar
Tallósy, SP, Janovák, L, Nagy, E, Deák, A, Juhász, A, Csapó, E, Buzás, N and Dékány, I(2016) Adhesion and inactivation of gram-negative and gram-positive bacteria on photoreactive TiO2/polymer and Ag–TiO2/polymer nanohybrid films. Applied Surface Science 371, 139150.CrossRefGoogle Scholar
Toews, MD, Campbell, JF and Arthur, FH (2010) The presence of flour affects the efficacy of aerosolized insecticides used to treat the red flour beetle Tribolium castaneum. Journal of Insect Science 10, 196.CrossRefGoogle ScholarPubMed
Tomasz, J (2015) Evaluation of the impact of pre-sowing microwave stimulation of bean seeds of the germination process. Agricultural Engineering 19, 4556.Google Scholar
Tyata, RB, Subedi, DP, Shrestha, A and Baral, D (2012) Development of atmospheric pressure plasma jet in air. Kathmandu University. Journal of Science and Engineering Technology 8, 1522.Google Scholar
Vadivambal, R, Jayas, DS and White, ND (2006) Disinfestation of life stages of Tribolium castaneum in wheat using microwave energy. 2006 ASAE Annual Meeting (p.1). American Society of Agricultural and Biological Engineers.CrossRefGoogle Scholar
Vadivambal, R, Jayas, DS and White, NDG (2007) Wheat disinfestation using microwave energy. Journal of Stored Products Research 43, 508514.CrossRefGoogle Scholar
Vadivambal, R, Jayas, DS and White, NDG (2008) Mortality of stored-grain insects exposed to microwave energy. Transactions of the ASABE 51, 641647.CrossRefGoogle Scholar
Vadivambal, R, Deji, OF, Jayas, DS and White, NDG (2010) Disinfestation of stored corn using microwave energy. Agriculture and Biology Journal of North America 1, 1826.Google Scholar
Valizadegan, O, Pourmirza, AA and Safaralizadeh, MH (2009) Combination of microwaves radiation and cold storage for control of Oryzaephilus surinamensis (L.)(Col. Silvanidae). Journal of Biological Sciences 9, 231236.CrossRefGoogle Scholar
Vijayavel, K and Balasubramanian, MP (2009) Effect of fenvalerate on oxidative stress biomarkers in the brackish water prawn Penaeus monodon. Pesticide Biochemistry and Physiology 95, 113116.CrossRefGoogle Scholar
Vontas, JG, Small, GJ and Hemingway, J (2001) Glutathione S-transferases as antioxidant defense agents confer pyrethroid resistance in Nilaparvata lugens. Biochemical Journal 357, 6572.CrossRefGoogle Scholar
Wang, S and Tang, J (2001) Radio frequency and microwave alternative treatments for insect control in nuts: a review. International Agricultural Engineering Journal 10, 105120.Google Scholar
Wang, S, Wang, J and Guo, Y (2018) Microwave irradiation enhances the germination rate of Tartary buckwheat and content of some compounds in its sprouts. Polish Journal of Food and Nutrition Sciences 68, 195205.CrossRefGoogle Scholar
Wu, RSS and Lam, PKS (1997) Glucose-6-phosphate dehydrogenase and lactate dehydrogenase in the green-lipped mussel (Perna viridis): possible biomarkers for hypoxia in the marine environment. Water Research 31, 27972801.CrossRefGoogle Scholar
Zhao, S, Qiu, C, Xiong, S and Cheng, X (2007) A thermal lethal model of rice weevils subjected to microwave irradiation. Journal of Stored Products Research 43, 430434.CrossRefGoogle Scholar
Zhou, R (2019) Direct and indirect activation of biological objects using cold atmospheric plasma. Ph. D. Thesis, School of Chemistry, Physics and Mechanical Engineering. Science and Engineering Faculty Queensland University of Technology, Brisbane, Queensland, Australia II.Google Scholar
Zhou, R, Zhou, R, Zhang, X, Zhuang, J, Yang, S, Bazaka, K and Ostrikov, KK (2016) Effects of atmospheric-pressure N2, He, air, and O2 microplasmas on mung bean seed germination and seedling growth. Scientific Reports 6, 32603.CrossRefGoogle ScholarPubMed
Zinhoum, RA, Negm, AA, Abd-El Hameed, SM and Afify, A (2019) Efficiency of some safe methods in controlling Stegobium paniceum on capsicum minimum plant. International Journal of Entomology Research 4, 0714.Google Scholar
Ziuzina, D, Los, A, Akkermans, S, Boehm, D, Cullen, PJ, Van Impe, JFM and Bourke, P (2018) Modelling microbiological and quality marker responses to enhance cold plasma cereal grain processing. Proceedings of the 10th International Conference on Simulation and Modelling in the Food and Bio-Industry, FOODSIM, 229–234.Google Scholar
Figure 0

Figure 1. The schematic diagram of DBD cell used as a stress for the control of T. castaneum and T. granarium adults and larvae.

Figure 1

Figure 2. Current voltage waveform for atmospheric pressure air plasma discharge at about (a) 9 KV and (b) 10 KV applied voltage.

Figure 2

Figure 3. Lissajous figures of air DBD plasma at about 9, 10, and 11 KV applied voltages.

Figure 3

Table 1. Effect of non-thermal APPD using air as a processing gas on the percentage mortality (mean ± SE) of T. castaneum adults and larvae 24 h and 7 days post-exposure to different powers at various time periods (sec)

Figure 4

Table 2. Effect of non-thermal APPD using air as a processing gas on the percentage mortality (mean ± SE) of T. granarium adults and larvae 24 h and 7 days post-exposure to different powers at various time periods (sec)

Figure 5

Table 3. Determination of the significant effect of exposure times and tested power level factors on the mortality percent of T. castaneum and T. granarium adults and larvae after 24 h and 7 days post-exposure to non-thermal APPD using air as a processing gas

Figure 6

Table 4. Factorial analysis for the general trend between the two pests, stages, and inspection times post-exposure to non-thermal APPD

Figure 7

Table 5. Effect of microwave energy on the percentage mortality (mean ± SE) of T. castaneum adults and larvae 24 h and 7 days post-exposure to different powers at various time periods (sec)

Figure 8

Table 6. Effect of microwave energy on the percentage mortality (mean ± SE) of T. granarium adults and larvae 24 h and 7 days post-exposure to different powers at various time periods (sec)

Figure 9

Table 7. Determination of the significant effect of exposure times and tested power level factors on the mortality percent of T. castaneum and T. granarium adults and larvae after 24 h and 7 days post-exposure to microwave

Figure 10

Table 8. Factorial analysis for the general trend between the two pests, stages, and inspection times post-exposure to microwave energy

Figure 11

Table 9. The expected exposure time (sec) caused 50 and 90% mortality for T. castaneum and T. granarium adults and larvae post-exposure to non-thermal APPD using air as a processing gas at different powers after 24 h and 7 days post-exposure

Figure 12

Table 10. The expected exposure time (sec) caused 50 and 90% mortality for T. castaneum and T. granarium adults and larvae post-exposure to microwave at different powers after 24 h and 7 days post-exposure

Figure 13

Table 11. Effect of non-thermal APPD at 15.9 W and microwave energy at 300 W on the germination% of wheat grains post-exposure to lethal exposure times at the 50 and 90% level of T. castaneum and T. granarium adults and larvae

Figure 14

Table 12. Changes in antioxidant enzyme activity and total proteins (mean ± SE) in T. castaneum and T. granarium adults and larvae 24 h after exposure to lethal exposure times 50% level at 15.9 W power level of non-thermal APPD using air as a processing gas