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Atmospheric Cold Plasma (ACP) Treatment for Efficient Disinfestation of the Cowpea Weevil, Callosobruchus maculatus
Nahndi Tirrell Kirk-Bradley1,*, Tomilayo Grace Salau1, Keyan Zhu Salzman2, Janie McClurkin Moore1,**
Published in Journal of the ASABE 66(4): 921-927 (doi: 10.13031/ja.15449). Copyright 2023 American Society of Agricultural and Biological Engineers.
1Biological and Agricultural Engineering, Texas A&M University, College Station, Texas, USA.
2Department of Entomology, Texas A&M University, College Station, Texas, USA.
Correspondence: *ntkirkbr@tamu.edu, **Janie.Moore@ag.tamu.edu
The authors have paid for open access for this article. This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License https://creative commons.org/licenses/by-nc-nd/4.0/
Submitted for review on 8 November 2022 as manuscript number PRS 15449; approved for publication as a Research Article by Associate Editor Dr. Akinbode Adedeji and Community Editor Dr. Sudhagar Mani of the Processing Systems Community of ASABE on 12 April 2023.
Highlights
Abstract. The insecticidal capability and mechanism of high-voltage atmospheric cold plasma were studied using a dielectric barrier discharge reactor against Callosobruchus maculatus, a significant insect pest in stored grain degradation. The mortality rate of > 90.0% for egg and larval stages can be achieved with a longer treatment time of 3 minutes and a higher voltage of 70 kV. However, this treatment condition, paired with a post-treatment retention time of 4 days, is required to kill 95% of adult insects. The use of atmospheric cold plasma has a considerable impact on the mortality of a range of insect life stages. Sufficient toxicity can be achieved by plasma process management using modified atmospheric pressure with a working gas of 65% oxygen, 30% carbon dioxide, and 5% nitrogen to address the insect lifecycle phases that are vectors for pathogens, which can increase mycotoxin contamination and degrade grain quality. Introducing atmospheric cold plasma treatment as an alternative to chemical fumigation may provide a safer alternative for integrated pest management.
Between 30% and 40% of food in the United States is reported to be lost to food waste (USDA, Food Waste FAQs). According to estimates from the United States Department of Agriculture Economic Research Service, this is approximately 133 billion pounds and $161.6 billion in food loss at the retail and consumer levels in 2010. One of the primary sources of this loss at the postharvest stage is pests and plant diseases, which account for 40% of global agricultural output losses (Mahmood et al., 2016). A large number of pest species are linked to stored commodities. (Stejskal et al., 2002). Numerous studies (Phillips and Throne, 2009; Wijayaratne et al., 2018; Mihale et al., 2009) show that stored product pests can damage, spoil, or consume as much as 10% of all food produced in developed nations and as much as 20% or more in developing nations. In humid environments, pests can account for up to 50% of food loss (Wijayaratne et al., 2018), while other studies have shown that pests are responsible for 10% to 60% of postharvest grain losses in developing nations (Mihale et al., 2009).
Pests attack stored grains more aggressively, causing considerable damage. Internally feeding insects consume the endosperm of grains, resulting in grain weight loss, nutritional value decline, quality deterioration, and seed viability and vigor reduction (El-Aziz et al., 2014). Insects that feed externally and internally can also cause harm to grains through feces contamination, empty eggs, larval molts, empty cocoons, and dead adult insects. Insects are also vectors for the development of fungal pathogens, which can increase mycotoxin contamination and lower grain quality, making grain quality preservation and food availability a constant concern (Richard-Molard, 2003; El-Aziz et al., 2014; Sutar et al., 2021).
Approximately 3 million tons of pesticides are used annually on a global scale, and almost 500 active chemicals are employed in plant protection products (Silva et al., 2019). Chemical insecticides, such as contact insecticides and fumigants, such as phosphine, are sprayed during all stages of plant development and crop storage to suppress insect pests (Bolzonella et al., 2019). Organophosphates, pyrethroids, organochlorines, and neonicotinoids are the most frequent contact insecticides used in cereal grain storage (Randhawa et al., 2014; Carvalho, 2017). As a result of the phasing out of methyl bromide, phosphine fumigation is frequently employed. However, it has drawbacks, such as lengthy exposure periods and ineffectiveness against many stored grain pests (Benhalima et al., 2004; Pimentel et al., 2008; Rajendran and Sriranjin, 2008). While pesticides serve a crucial role in crop protection, their widespread use and nontarget toxicity may have long-term effects on ecosystems, people, and other living things, and contribute to the evolution of insect resistance (Silva et al., 2019; Carvalho, 2017; Benhalima et al., 2004; Pimentel et al., 2008; Rajendran and Sriranjin, 2008).
Insects are one of the most damaging animal pests to stored grains because they are exceptionally adaptive to low nutritive conditions and are typically regarded as perpetual pests (Rajendran and Sriranjin, 2008; Richard-Molard, 2003). The Callosobruchus genus contains some of the most destructive pest species in tropical and subtropical environments (Giga and Smith, 1983). Callosobruchus maculatus (Coleoptera: Chrysomelidae), the cowpea weevil, is a significant pest of grain legumes both in storage and in the field, most typically under storage circumstances. This species originated in Africa and is now distributed across the tropics and subtropics. C. maculatus mostly targets beans of diverse types, although it can also damage other pulse crops. This species is a significant pest of economically important grain legumes like cowpea, lentil, green gram, and black gram (Park et al., 2003). Cowpea weevils are internal feeders that lay eggs on the seed surface in the field and during threshing, which hatch during storage. When favorable conditions become available, the pest multiplies. When the larva feeds within the beans, it may leave nothing but the shell, resulting in considerable weight loss, nutritional value decline, and germinability. (Atanda et al., 2016). This adds greatly to the financial costs of the food production industries (Yao et al., 2019). Aside from economic concerns, weevils emit harmful quinones and carcinogens, putting consumers' health and safety at risk (Deb and Kumar, 2020). To ensure long-term environmental stability and optimum agricultural yields, innovative control strategies are urgently needed to address consumer concerns, environmental consequences, and developing insect resistance.
A number of studies examined alternatives to pesticides (Huang et al., 2005; Kedia et al., 2015; Souto et al., 2021), including plant-derived natural components (Dubey et al., 2008), insect growth regulators (Tunaz et al., 2004), ozone (McDonough, 2010), and atmospheric cold plasma (ACP). ACP is a nonthermal treatment technology that uses energetic, reactive gases to kill pathogens on meats, poultry, fruits, and vegetables (Han et al., 2016; Chaplot, Shreyak, et al., 2019; Rana, Sudha, et al., 2020; Moiseev et al., 2014). This versatile sanitizing approach employs electricity and a carrier gas such as air, oxygen, nitrogen, or helium (Moiseev et al., 2014). No antibacterial chemical compounds are required. Ultraviolet photons, balanced negative and positive ions, free radicals, and free electrons make up ACP, which is produced at atmospheric pressure and has low or no temperature effects on target foods (M. Ferreira et al., 2016). ACP uses a variety of processes to combat biocontamination and sustainability challenges in the food and agriculture industries. These qualities provide a rich resource for developing alternative agricultural commodity preservation solutions to existing fumigation procedures.
However, as an insecticidal technique, it is still relatively underexplored and insufficiently understood. The goal of this study was to examine the insecticidal capability of ACP treatment using the cowpea weevil, C. maculatus, as an insect model. This study employs a well-characterized cold plasma processing device that employs modified atmospheric pressure (MAP) (65% oxygen, 30% carbon dioxide, and 5% nitrogen) as the inducer gas, in addition to process and system research results to date, in order to refine and comprehend how this scalable approach can be used for insect control to promote food security. The impact of plasma process factors such as treatment duration, varied voltages, and post-treatment retention time (PTRT) on insecticidal efficacy was assessed using the mortality of insects at various developmental stages, such as egg, first instar larvae, and adults.
Materials and Methods
Conditions for Insect Rearing and Sample Preparation
C. maculatus was collected from a colony kept in the Department of Entomology at Texas A&M University in College Station, Texas. They were reared in glass jars on 75 grams of cowpea seeds (Vigna unguiculata) at room temperature with a relative humidity of 60 ± 5% in the dark at 27 ± 1 °C (Arant, 1938). Porous Kimtech Wipes were used to prevent adult insects from escaping. The insecticidal effects of ACP were studied using C. maculatus 48 hour-old eggs, first instar larvae (1-2 weeks old), and non-mated adults (6 weeks old). Adult insects were incubated on 75 grams of cowpea seeds for 24 hours at 27 ± 1°C to mate. Adult insects were removed after incubation, and eggs were collected and incubated at 27 ± 1°C for an additional 24 hours.
Atmospheric Cold Plasma System Setup
The ACP system employed in this investigation was a high-voltage (HV) dielectric barrier discharge (DBD) device with a maximum voltage output in the range of 0-120 kVRMS at 50 Hz, which has been described in detail by Pankaj et al. (2013) and extensively characterized by Moiseev et al. (2014). The schematic diagram of the ACP system setup is shown in figure 1. The samples were exposed to confined ACP treatment at 20, 50, and 70 kV at modified atmospheric pressure with a working gas of 65% oxygen, 30% carbon dioxide, and 5% nitrogen. The overall distance between the two 15 mm aluminum disc electrodes was roughly 50 mm, which was equal to the dimensions of the polypropylene container (Petri dish) used as a sample holder (63mm x 8.5mm) and the thicknesses of the top (10 mm) and bottom (7 mm) dielectric barriers. Samples were put in a Petri dish and exposed to plasma in a direct (inside the area of plasma discharge) method. Each petri dish was sealed within a polypropylene Cryovac bag (SEALED AIR, Charlotte, NC) filled with the working gas (40-50 mm in depth) prior to treatment to contain plasma-generated reactive gas species (ROS) within the bag.
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| Figure 1. Schematic of experimental lab setup using dielectric barrier discharge atmospheric cold plasma system. |
Atmospheric Cold Plasma Treatment
To evaluate the insecticidal effects of ACP on C. maculatus eggs and first instar larvae, a ULINE S-18514 round magnification lens was used to count the insects on top of and within the seeds' endosperm. Twenty eggs, first instar larvae (with seed counts ranging from 6 to 10), and ten adult insects were placed in Petri dishes, and exposed to 0-3 minutes of treatment at 0, 20, 50, and 70 kV, respectively. After the samples were treated, they were left inside the Cryovac bag with reactive gas species (RGS) for 30 minutes to allow the RGS to permeate the bag. The insect samples were then put back into the jars, and various post-treatment retention times were observed. To conduct the study, we used 48-hour-old egg samples. In the fourth week following oviposition, we examined first-instar larvae samples to determine whether they had progressed to the fourth instar, which is characterized by the larvae turning a darker color and creating translucent windows. We recorded any instances where this development did not occur. We then waited for an additional two weeks to see if the insects emerged and declared them dead if no emergence occurred. For adult insects, we used specimens aged 3-5 days. The control groups consisted of eggs, first instar larvae, and adult insects. These control samples were maintained under identical experimental conditions as the treated insects, with the exception of plasma exposure. The controls followed standardized protocols for PTRTs, housing, and location. Each experiment, which included eggs, first instar larvae, and adult insects, was repeated three times.
Insect Analysis
Viability Assay
The effect of ACP treatment on C. maculatus viability was measured in terms of percentage mortality. All insect samples were inspected visually with a ULINE S-18514 round magnifying lens. To examine if ACP had any impact on C. maculatus egg mortality, the eggs were left inside the Cryovac bag with reactive gas species (RGS) for 30 minutes after treatment to allow the RGS to permeate the bag before being put back into glass jars and kept at 27 ± 1°C for 7 days to see if they would hatch into larvae. The egg mortality was estimated as the number of unhatched eggs/total number of eggs per experiment multiplied by 100%. First instar larvae were given corresponding treatments before being transferred back into glass jars to be incubated at 27 ± 1°C for up to 4 weeks to see if the larvae would move to the pupae phase. For adult insects, the samples were treated and remained inside the Cryovac bag for 30 minutes with RGS before being placed into C. maculatus rearing medium of 75 g of cowpea seeds in glass jars and incubated for 7 days at 27 ± 1°C. The observation was repeated for both moribund and surviving adult insects from Day 0 to Day 7. Insects were deemed dead if they did not move. To assess the effect of ACP on larvae in their first instar, treatment samples were incubated until adult emergence was seen (approximately 6 weeks). First instar larvae mortality was measured as the number of non-emergence insects/total number of insects for each experiment multiplied by 100%. Adult insect mortality was measured as the number of dead insects divided by the total number of insects in each experiment.
Statistical Analysis
SPSS Statistics was used for statistical analysis (version 27.0.1.0, IBM Software, Inc.). The means of all ACP treated samples and the corresponding untreated controls were analyzed and compared using the Fisher's least significant difference method at the 0.05 confidence level.
Results and Discussion
Effect of ACP on the Viability of Cowpea Weevils
The direct mode of plasma exposure yielded the highest hatch rate mortality of 91% for treated eggs at 70 kV for 3 minutes, compared to a 10% hatch rate mortality for controls. Hatch rate mortality is when the eggs do not hatch into larvae. On day 7, the samples were studied to determine if the treated samples had hatched or died. For the control samples of 0 minutes (each voltage sample had its own set of controls), the hatch rate mortality was less than 20% (fig. 2).
Mortality of Egg Life Stage
The hatch rate mortalities for eggs at 1 min for 20, 50, and 70 kV corresponded to 0%, 38%, and 58%, respectively. The hatch rate mortalities for treated egg samples at 2 min for 20, 50, and 70 kV corresponded to 23%, 49%, and 73%, respectively. The hatch rate mortalities for treated egg samples at 3 min for 20, 50, and 70 kV corresponded to 37%, 54%, and 91%, respectively. The sensitivity of C. maculatus egg mortality hatch rate to atmospheric cold plasma (ACP) depended on the duration of treatment and the amount of voltage. The mortality of C. maculatus increased with increasing treatment time and voltage, which agrees with other reports focusing on the insecticidal effects of plasma (Ziuzina et al., 2021; Donohue et al., 2006; Hassan et al., 2020). Higher mortality rates of insects across the different life stages were achieved with direct plasma exposure. Prior research focusing on the insecticidal effects of plasma shows that direct treatment yields more insect mortality than indirect plasma exposure (Ziuzina et al., 2021).
Mortality of First Instar Larvae Life Stage
For first instar larvae, results were similar to those of egg mortality hatch rates. Direct plasma exposure, with longer treatment times and higher voltages, yielded a higher mortality rate. The mortality rates for treated first instar larvae samples at 20 kV for 1, 2, and 3 minutes corresponded to 17%, 57%, and 82%, respectively (fig. 3). The mortality rates for treated first instar larvae samples at 50 kV for 1, 2, and 3 minutes corresponded to 18%, 65%, and 89%, respectively (fig. 3). The mortality rates for treated first instar larvae samples at 70 kV for 1, 2, and 3 minutes corresponded to 22%, 76%, and 93%, respectively (fig. 3). Direct exposure to plasma treatment significantly reduced (p <.05) the viability of eggs and first instar larvae.
Mortality of Adult Life Stage
However, adults proved to be more difficult to kill. Much longer treatments were required to kill adult insects, but more pronounced effects of PTRT were noted, suggesting a different emphasis on the mechanisms of inactivation. Direct plasma exposure treatment at 1, 2, and 3 minutes for 20, 50,
and 70 kV, respectively, were applied to adult insects. The mortality rate for treated adult samples at 20, 50, and 70 kV for 1, 2, and 3 minutes, respectively, started to decline after 24 hours compared to a 0% mortality rate for controls. By day 5, direct exposure to ACP for 3 minutes at 70 kV resulted in 100% mortality, compared to 0% mortality in non-treated insects (fig. 4). On days 6 and 7, direct exposure to ACP for 3 minutes at 70 kV resulted in 100% mortality, compared to 0% mortality in non-treated insects. These results suggest that control of adult insects can be achieved by combining higher voltage, longer treatment times, and PTRT. The average life expectancy for an adult mature C. maculatus in our lab environment was approximately 11-12 days, which is comparable to field study findings of 10-14 days (Giga and Smith, 1983), indicating that ACP treatment reduces C. maculatus lifespan.
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| Figure 2. The effect of direct plasma exposure on the viability of C. maculatus eggs. Mortality of the eggs is displayed as a function of treatment time and voltage on day 7, when eggs did not hatch into first instar larvae. The 0 represents the control populations. There was a set of controls for each voltage of 20, 50, and 70 kV. Standard deviation is denoted by error bars. Different letters indicate significant differences at n = 20 (p <.05). |
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| Figure 3. The effects of direct plasma exposure on the viability of C. maculatus first instar larvae. Mortality of the larvae is displayed as a function of treatment time and voltage at day 42 (6 weeks) when first instar larvae did not emerge into adults. Standard deviation is denoted by error bars. Different letters indicate significant differences at n = 20 (p <.05). |
In this study, direct exposure to plasma was applied. Direct exposure is the combined attack of produced charged particles, UV, and short- and long-lived plasma reactive species on target organisms (Ziuzina et al., 2021). The RGS from the plasma, in general, breaks down cell walls, doubles lipid bonds, and allows RGS to destroy intracellular structures. By causing strong responses to the applied field, the reaction mechanisms involve the vibration, excitation, dissociation, attachment, and ionization of the molecular species. There are studies to support the inactivation of Aspergillus flavus using ACP by showing that there was cell leakage and loss of viability (Suhem, et al., 2013). This same mechanism may apply to insects. The exposure to the reactive species has shown that post ACP treatment, the conidiophores and the vesicles were broken, resulting in a loss of cellular viability. Similarly, the double lipid layers in the cell are disrupted, allowing RGS to react with the inner cellular structures. Our findings are directly applicable to the treatment of stored grain commodities and are consistent with previous studies (Los et al., 2018; Suhem et al., 2013; Los,
2017), which demonstrated that the manner of plasma exposure and PTRT in a controlled environment were important factors in achieving biocidal effects. Prior studies utilizing ACP on pests have focused on Tribolium castaneum at various phases of development to discover the treatment parameters for ACP treatment. The use of ACP on T. castaneum mortality was demonstrated utilizing brief treatment intervals ranging from 0.5 to 5 minutes, with adults being the most resistant stage to direct treatment (Ziuzina et al., 2021). Another study discovered that after being subjected to sublethal ACP treatments, adult populations' respiration rates were lowered, and that this was positively associated with insect weight (Ziuzina et al., 2021). As a result, the levels of lipid peroxidation and GST activity increased as the treatment period increased.
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| Figure 4. The effects of direct plasma exposure on the viability of C. maculatus adults. Percent survival of the treated adults is displayed as a function of treatment time, voltage, and corresponding PTRT of 0-7 days. The means of all adult insect-treated samples and untreated controls were subjected to analysis of variance and compared using Fisher's technique of least significant difference at the 0.05 confidence level. |
This study found comparable results in C. maculatus treated with ACP. The hypothesis in this study was validated because changing the ACP system parameters had an effect on C. maculatus, resulting in insect death. Higher voltages, treatment durations, and PTRT for adults had the most impact. Lower voltages and shorter treatment durations, on the other hand, had fewer effects. The goal of evaluating the efficacy of ACP treatment on three critical life stages of C. maculatus (egg, first instar, and adult) was accomplished. The results indicated how multiple lifecycle stages might impact effective inactivation. Further research into other insect pests and their different lifecycle stages is recommended in order to uncover viable uses of ACP for integrated pest control methods across the agriculture industry.
Potential Effect of RGS and Plasma Treatment
Another finding from this study was the effect of plasma-produced reactive gas species (RGS) on C. maculatus discoloration. RGS can cause hydrocarbon breakdown in the cuticular lipid layer of insects, as well as dehydration and mortality (Ramanan et al., 2018). This study demonstrated empirical evidence of this phenomenon through the
observed shift in hue from brown to dark black, as depicted in figure 5. Our study investigated the effect of atmospheric cold plasma treatment on the discoloration of adult cowpea weevils. We found that, before homogenization, there were no observable changes in the treated weevils. However, there was a noticeable pigmentation shift following treatment. This could be due to pigment breakdown from plasma bleaching (Byun et al., 1997). Previous studies have shown that ozone treatment can cause significant changes in fatty acid content and the destruction of natural pigments (Byun et al., 1997), and dehydration can influence the body color of mature C. maculatus, with hydrated populations being substantially darker than dehydrated populations (Noh et al., 2015). Additionally, a recent study on pea aphids showed that changes in body color were connected to changes in pigment composition and concentration under stress (Wang et al., 2019). The researchers suggest that this could be an adaptation mechanism to environmental stress and a way to store and utilize energy reserves. Further research is needed to determine whether similar mechanisms are at play in C. maculatus treated with atmospheric cold plasma. Our key finding is that atmospheric cold plasma treatment can cause a noticeable pigmentation shift in adult cowpea weevils, which may have implications for understanding how this treatment affects insect physiology.
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| Figure 5. Non-treated adult cowpea weevils vs. treated adult cowpea weevils at 70 kV for 3 minutes. |
Conclusions
Controlled HVACP treatment under modified atmospheric pressure with a carrier gas of 65% oxygen, 30% carbon dioxide, and 5% nitrogen proved effective against C. maculatus, demonstrating the potential of grain stability in storage. A longer treatment period of 3 minutes and a higher voltage of 70 kV resulted in > 90.0% for egg and larval stages. However, to kill 100% of adult insects, a longer plasma exposure (3 minutes) at a higher voltage (70 kV) combined with a post-treatment retention duration of 5 days is necessary. Given the adaptation and resistance mechanisms of insects, more research is needed to understand long term plasma effects as well as how to commercialize and register this treatment technology as a viable component for integrated pest management in the agricultural industry.
Acknowledgments
A special thanks to Tomilayo Salau, a Texas A&M University undergraduate student who was instrumental in helping do the hands-on work in the lab for this research study. This project was also supported by NC-213, the United States Quality Grains Research Consortium.
Nomenclature
ACP = Atmospheric cold plasma
RGS = Reactive gas species
PTRT = Post-treatment retention time
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