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Comparative analysis of active period and oxidative stress of DDVP and ginger (Zingiber officinale) oil on Indian meal moth (Plodia interpunctella Hübner) infesting maize grain

The Journal of Basic and Applied Zoology volume 85, Article number: 50 (2024) Cite this article

Abstract

Background

Indian meal moth (Plodia interpunctella) is a significant pest infesting stored grains, particularly maize. Over time, synthetic insecticides have been employed to control insect. The residual effects posed on non-target organisms have called for replacement of synthetic insecticides with botanicals. This study therefore aimed at comparing the insecticidal consistency and oxidative stress invoked by dichlorvos (DDVP) and the oil extract of ginger (Zingiber officinale) on Indian meal moth infesting maize. Disinfested maize grains were treated with DDVP and ginger oil extract separately. Adults P. interpunctella were introduced to the treated grains daily using complete replacement method. The percentage mortality was calculated daily for 10 d. Furthermore, the oxidative stress caused by DDVP and ginger oil extract on the moth was evaluated by measuring the level of some oxidative stress biomarkers such as glutathione S-transferase, superoxide dismutase, glutathione peroxidase (GPx), and catalase (CAT) activity in the exposed insects.

Results

Preliminary results indicated that both DDVP and ginger oil extract exhibited insecticidal properties against Indian meal moth infesting maize. However, the insecticidal (active) period of ginger oil extract was found to be longer than that of DDVP. Nevertheless, DDVP provoked greater oxidative stress in the exposed moth.

Conclusions

Ginger oil extract and DDVP show potential for controlling Indian meal moth infestations in stored maize. Yet, ginger oil offers a longer-lasting effect on pest suppression and control. Consequently, it could be a replacement or synergistic insecticide with DDVP to provide ecofriendly insecticide application.

Background

Insecticides are chemical substances applied in small quantity to control insects. The choice of insecticide depends on several factors to include potency to control insects, duration of active period, and environmental safety. The consistency of the active ingredients in insecticide is time dependent because most insecticide tends to become less active to the target insects after few days of application. Based on environmental safety, particularly on non-target organisms, United States Environmental Protection Agency (Bourguet & Guillemaud, 2016) reported spending more than $100 billion (per year) to control the effect of insecticides on non-target organisms and the environment. (Abdullha, 2016; Kataria & Kumar, 2012). The paradigm shift from synthetic insecticides to botanical insecticides is welcome due to the side effects and cost of production of synthetic insecticides (Tavares et al., 2010; Mossa et al., 2018). Many botanicals such as Plumbago zeylanica, Cymbopogon citratus, Z. officinale, etc. (Adeyera & Akinneye, 2020; Oyeniyi et al., 2022; Salami & Olufemi-Salami, 2017), have shown a promising future in the control of stored product insects (Abdulhay & Yonius, 2019; Adeyera & Akinneye, 2020; Fernandes, 2012) Although synthetic insecticides raise farmers’ hope in insects control, the environmentalists have great concern on synthetic insecticides’ resistance and lingering impacts on the ecosystem, particularly on non-target organisms (Varma & Dubey, 1999; Jeyasankar & Jesudasan, 2001, Ahmad and Arif, 2010; Giambo et al., 2021). Hence, there is a need to substitute synthetic insecticides with ecofriendly botanicals insecticides.

Ginger root oil has been reported to have insecticidal properties against a wide range of insect pests, including P. interpunctella (Bhattacharjee et al., 2019; Choo et al., 2010). The insecticidal properties of ginger root oil are attributed to the presence of various compounds, including gingerols, shogaols, and zingerone, which have been shown to have toxic effects on insects (Yongxing et al., 2023). Dichlorvos commonly referred to as DDVP is a widely used synthetic insecticide. It has been reported to be effective in controlling stored grain pests, including P. interpunctella (Olufemi-Salami et al., 2023; Suthisut et al., 2011). However, the use of DDVP has been associated with the development of resistance in insect populations, and there are concerns about its toxicity on non-target organisms (Liu et al., 2019). Acevedo et al., (2009) reported the resistance of housefly (Musca domestica) to DDVP, likewise, Ranian et al., (2021) reported the resistance dipterans to some pyrethroid and organophosphate.

Generally, most insecticides act as a xenobiotic causing the release of free radicals that possibly result in oxidative stress. Oxidative stress measured through antioxidant enzyme activity has been used to determine the degree of stress or toxicity of insecticides (Zhao & Haddad, 2011; Possik & Pause, 2015; Rivera-Ingraham & Lignot, 2017; Dongxing, 2019; Kramer 2021). Most commonly measured antioxidant enzymes are superoxide dismutase (SOD), catalase (CAT), glutathione peroxidase (GPx), and glutathione S-transferase (GST). Although many researches have reported ginger as a potential insecticide, little is documented or known on the active period of ginger and its ability to act as an oxidative stressor in moth. Therefore, this research aimed at comparing the active (consistency) period and level of oxidative stress caused by DDVP and ginger oil extract in Indian meal moth infesting maize grains.

Methods

The maize variety TZESR-20 was obtained from the Agricultural Development Programme, Akure, Nigeria. The Z. officinale rhizome was purchased at the king’s market (Oja Oba), Akure, Ondo State. Also, the DDVP used was obtained from the Agricultural Development Programme Centre (ADPC), Akure.

Plant materials preparation

The Z. officinale rhizomes were purchased in Oba market, Akure, Ondo State, and brought to the laboratory of Storage Research Laboratory, Department of Biology, Federal University of Technology Akure, Ondo state, Nigeria. The Z. officinale rhizomes were sliced and then air-dried. The dried slices of the rhizome were pulverized into fine powder using a Binatone Electric Blender (Model 373). The pulverized powder was stored in plastic containers with airtight lids for subsequent use.

Plant oil extraction

Two hundred grams of the pulverized plant materials were poured into a muslin cloth of dimension 50 × 50 cm and then transferred into the thimble and extracted with ethanol in a soxhlet apparatus model 77–520 (Hospital Equipment Manufacturing Co. Limited, India). The extraction was carried out for 3–4 h. It was terminated when the solvent in the thimble became clear. Then the thimble was removed from the unit and the solvent recovered by distilling in the soxhlet extractor. The Rotary evaporator was used to separate the solvent from the oil after collection of the resulting extracts from the soxhlet, after which the oil was exposed to air so that traces of the volatile solvent evaporate, leaving the oil extract. The resulting oil was kept in glass bottles and stored at 4 °C until required for use (Adegbe et al., 2016).

Insect culture

The P. interpunctella used to establish the culture were obtained from naturally infested maize grains from the Storage Research Laboratory, Department of Biology, Federal University of Technology Akure, Ondo State, Nigeria. The moth’s larvae were reared in one-litre kilner jar containing 300 g of uninfected maize grains. The culture was maintained by continually replacing the devoured powder and sieving out frass and fragment. The kilner jar was covered with muslin cloth, fastened with rubber band, and placed inside a wire mesh cage of the dimensions 75 cm × 50 cm × 60 cm (L × W × H). The stands (legs) of the cage were dip in water–kerosene mixture contained in a plastic container, to prevent the entry of predatory ants. The culture was maintained at a temperature of 28 ± 2 °C and a relative humidity of 75 ± 5%. The whole setup was left inside the breeding cage in the laboratory.

Active period of DDVP and Z. officinale oil extract on adult P. interpunctella

Twenty grams of maize grains was treated with 0.1% of the concentration of the prepared concentrate of the insecticide. The concentrate was prepared by measuring 99.9 ml of water into 0.1 ml of DDVP. Then, ten freshly emerged adult P. interpunctella were introduced into plastic containers (8 cm diameter and 4 cm depth) covered with muslin cloths, using sterile carmel brush. The adult insects introduced into the treated maize grains were replaced daily with freshly emerged adult insects. The percentage mortality for each day was recorded up to 10 days post treatment of the grains. The same procedures were repeated using 0.2, 0.3, 0.4 and 0.5% concentration of DDVP for the treatment of the grains. Similarly, 0.1, 0.2, 0.3, 0.4 and 0.5% of the oil extract were also used as treatments and ethanol used as diluting solvent. Each of the experimental setup was replicated thrice and control experiment (treatment without DDVP or oil extract of Z. officinale) was set up.

Biochemical assay

Exposure of P. interpunctella

Adults and larvae (ten each) of P. interpunctella were exposed (in vivo method) to different percentage concentrations (0.1, 0.2, 0.3, 0.4 and 0.5%) of DDVP and oil extract of Z. officinale separately for 24 h, with three replicates for each treatment. The oxidative stress induced by the different percentage concentrations of DDVP and ginger oil treatments was then quantified in the lepidopteran.

Preparation of whole-body homogenates of the P. interpunctella

The whole-body homogenate was prepared by grinding the insects in 0.1 M phosphate buffer pH 7.0 using mortar and pestle. The mixture of the homogenate was centrifuged at 10 000 × g for 10 min with mini centrifuge machine C-M 1008 to obtain clear supernatant. The supernatants were decanted into sample bottles and were stored in the freezer until needed for enzyme assays.

Glutathione transferase activity assay

The method of Habig et al. (1974) with some modification was used to measure the glutathione transferase (GST) activity. The activity of GST was measured by observing the reaction involving the conjugation of CDNB with GSH forming a coloured conjugate glutathione 2, 4- dinitrobenzene. For measurement, the reaction mixture contained 0.1 M sodium phosphate buffer (pH 7.4), 10 mM GSH, 10 mM CDNB, and 0.2 mL tissue supernatant. Enzyme solution was added to 300 µl of GSH and 120 µl of CDNB in buffer. The reaction was allowed to progress at 340 nm for 3 min. The enzyme activity was calculated as µmol CDNB conjugate formed/min using a molar extinction coefficient of 9.6 × 103 M−1 cm−1 at 340 nm.

Superoxide dismutase activity assay

The activity of superoxide dismutase (SOD) was evaluated according to the method of Misra and Fridovich, (1972). Tissue supernatants were added to 2.5 ml of 0.05 M carbonate buffer (pH 10.2) to equilibrate in the spectrophotometer and the reaction was started by the addition of 0.3 ml of freshly prepared adrenaline (0.3 mM) to the mixture which was quickly mixed by inversion. The reference cuvette contained 2.5 ml of buffer, 0.3 ml of substrate and 0.2 ml of water. The increase in absorbance at 480 nm was monitored every 30 s for 150 s. One unit of SOD activity was given as the amount of SOD necessary to cause 50% inhibition of the oxidation of adrenaline to adrenochrome during 1 min.

Catalase activity assay

Catalase activity was assayed by the method of Clairborne (1985). This method is based on the disappearance of H2O2. The reaction volume contained 0.1 M sodium phosphate buffer (pH 7.4), 0.05 M H2O2, and 0.05 mL supernatant prepared from 10% tissue supernatant. Change in absorbance was recorded kinetically at 240 nm. CAT activity was calculated in terms of l mol H2O2 consumed/min using a molar extinction coefficient of 39.6 M−1 cm−1.

Glutathione peroxidase activity assay

Glutathione peroxidase (GPx) activity was determined by the method of Paglia and Valentine, (1967). A mixture of enzyme solution and buffer was added to 100 µL of GSH in test tubes containing nicotinamide adenine dinucleotide phosphate (NADPH) and glutathione reductase, 100 µl of H2O2 was then added to the mixture (containing supernatant of homogenate of tissue) to initiate the reaction. The reaction was monitored at 340 nm for 3 min on the UV–Visible spectrophotometer. The principle of determination is based on the decrease in absorbance of NADPH at 340 nm, and the activity was expressed as mmol NADPH/min/ml.

Data analysis

The significant differences in the means were determined using one-way analysis of variance using new Duncan’s multiple range test at P = 0.05 on Statistics Package for Social Sciences (SPSS) version 21. Chart was obtained using Microsoft Excel.

Results

The comparison of the active periods of DDVP and oil extract of Z. officinale is represented in Figs. 1, 2, 3, 4 and 5. At the first day of introduction of the insects, DDVP achieved 93.33% mortality, whereas the oil extract achieved only 13.33% mortality. Higher significant percentage mortality was recorded in the first and second day in DDVP treatment at all concentrations considered. At day 3, a sharp significant decrease was observed in the percentage mortality of the adult moths exposed to DDVP at all the concentrations considered. The percentage mortality for DDVP at day 3 was also observed to be less than 50%. The oil extract maintained it toxicity throughout the days considered. Moreover, a slight significant increment in the percentage mortality was observed as the posttreatment day increases. for achieved 26.67% a value that is 23.33% higher than the mortality achieved in DDVP at the same day. After day 6, the percentage mortality of the moth attained by the oil extract was higher than DDVP. At day 10, the toxicity of DDVP was lowest, whereas the oil extract still achieved percentage mortality of above 20%.

Fig. 1
figure 1

Comparison of active period of DDVP and Z. officinale oil at 0.1% Concentration. Vertical lines across straight lines represent standard error. Mean points with the same coloured line and letters are not significantly different at P = 0.05

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Fig. 2
figure 2

Comparison of active period of DDVP and Z. officinale oil at 0.2% Concentration. Vertical lines across straight lines represent standard error. Mean points with the same coloured line and letters are not significantly different at P = 0.05

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Fig. 3
figure 3

Comparison of active period of DDVP and Z. officinale oil at 0.3% Concentration. Vertical lines across straight lines represent standard error. Mean points with the same coloured line and letters are not significantly different at P = 0.05

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Fig. 4
figure 4

Comparison of active period of DDVP and Z. officinale oil at 0.4% Concentration. Vertical lines across straight lines represent standard error. Mean points with the same coloured line and letters are not significantly different at P = 0.05

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Fig. 5
figure 5

Comparison of the active period of DDVP and Z. officinale oil at 0.5% Concentration. Vertical lines across straight lines represent standard error. Mean points with the same coloured line and letters are not significantly different at P = 0.05

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Figures 6 and 7 show the results of the comparison of the glutathione transferase (GST) measured larvae and adults of Indian meal moth exposed to maize grains treated with DDVP and oil extract separately. The activities of enzyme GST at 0.1, 0.2, 0.3, 0.4 and 0.5% DDVP treatments were 106.48, 76.39, 74.07, 60.88 and 74.08 µmol/min/ml respectively, whereas the GST activities at 0.1, 0.2, 0.3, 0.4 and 0.5% of Z. officinale oil extract treatments were 209.26, 282.40, 310.42, 168.98 and 129.67 µmol/min/ml respectively. The activity of GST was higher in larvae exposed to oil extract treatment than those exposed to DDVP. However, the adult moths of DDVP treatment experienced more GST activities than the adults of the oil extract treatment (Figs. 6 and 7). Furthermore, the activity of superoxide dismutase (SOD) was higher in larvae of DDVP treatment than that of Z. officinale oil extract treatments. The activity of SOD was higher in adult moths of oil treatment than that of DDVP treatment (Figs. 8 and 9). The glutathione peroxidase (GPx) activity favours the larvae of oil treatment and adult P. interpunctella of DDVP treatment. The catalase (CAT) activity was higher in DDVP-treated larvae and adults than oil extract treatment (Figs. 10 and 11). The catalase activity was higher in larvae exposed to the oil extract than those exposed to DDVP when the insecticides were used as contact insecticide. However, when the insecticides were used as fumigant insecticides, DDVP provoked more catalase activity (Figs. 12 and 13).

Fig. 6
figure 6

Comparison of contact effect of DDVP and Z. officinale’s oil on GST activities in larva P. interpunctella. Line above bar is standard error. Means of same pattern and letters are not significantly different at P = 0.05

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Fig. 7
figure 7

Comparison of fumigant effect of DDVP and Z. officinale’s oil on GST activities in adult P. interpunctella. Line above bar is standard error. Means of same pattern and letters are not significantly different at P = 0.05

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Fig. 8
figure 8

Comparison of contact effect of DDVP and Z. officinale’s oil on SOD activities in larva P. interpunctella. Line above bar is standard error. Means of same pattern and letters are not significantly different at P = 0.05

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Fig. 9
figure 9

Comparison of fumigant effect of DDVP and Z. officinale oil on SOD activities in adult P. interpunctella. Line above bar is standard error. Means of same pattern and letters are not significantly different at P = 0.05

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Fig. 10
figure 10

Comparison of contact effect of DDVP and Z. officinale oil on GPx activities in Larva P. interpunctella. Line above bar is standard error. Means of same pattern and letters are not significantly different at P = 0.05

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Fig. 11
figure 11

Comparison of fumigant effect of DDVP and Z. officinale oil on GPx activities in Adult P. interpunctella. Line above bar is standard error. Means of same pattern and letters are not significantly different at P = 0.05

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Fig. 12
figure 12

Comparative effect of DDVP and Z. officinale oil on CAT activities in Larva P. interpunctella. Line above bar is standard error. Means of same pattern and letters are not significantly different at P = 0.05

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Fig. 13
figure 13

Comparison of fumigant effect of DDVP and Z. officinale oil on CAT activities in Adult P. interpunctella. Line above bar is standard error. Means of same pattern and letters are not significantly different at P = 0.05

Full size image

Discussion

Dichlorvos (DDVP) and oil extract of Z. officinale root proved high insecticidal activity against P. interpunctella infesting maize at a very low concentration. The two insecticides (DDVP and oil extract of Z. officinale) achieved different percentage mortality at same duration and concentration. This report is similar to the report by (Hamada et al., 2018 Madreseh-Ghahfarokhi et al., 2018; Sun et al., 2019 and Zhang et al., 2021) who described synthetic insecticide as very potent chemicals that could achieve high mortality rate within a short period of its application. Nevertheless, refined botanical has also shown promising insecticidal efficacy as reported by (Guleria & Tiku, 2009; Lengai et al., 2020).

Synthetic organophosphate insecticide, such as DDVP, is widely used for pest control due to its quick action and effectiveness. Nevertheless, the consistency of DDVP is fleeting and could achieve acute toxicity effectively only within three days of its application as observed in the result. The short-lived period of acute toxicity of DDVP could have been considered as part of safety precaution to reduce residual effect especially on non-target organism (Yadav & Devi, 2017). Therefore, a deliberate formulation of insecticide to facilitate the disintegration of active ingredient within 96 h of its application after which it might have achieved its insecticidal property might be responsible for the short active period of the DDVP. This observation is similar to the report by Manahan (2005) and Musa et al. (2010) who reported that synthetic insecticides are formulated to reduce environmental contamination; therefore, it could be broken down within a short range of its application (Yule, 1967; B‐Bernard and Philogène, 1993; Moffat, 1993).

The consistency of acute toxicity of Z. officinale oil extract on P. interpunctella over a period of 10 d might be as a result of its botanical origin, high content of natural antioxidant and the presence of highly stable ligand in the botanical oil. This submission is similar to the report by (Weinzierl, 1999 and Dubey 2010) who reported the presence of antioxidant as a major factor influencing the shelf life and active period of botanical oil. Furthermore, the oil extract of ginger root has been reported to have a longer active period, ranging from 3 to 6 weeks (Rondanelli et al., 2020 and Zhang et al., 2021).

The redox imbalance created by DDVP and oil extract of ginger quantified through the activity of antioxidative enzymes (GST, SOD, GPx and CAT) shows both downward and upward regulations. The comparison of both insecticides did not outrightly favour the botanical oil over the synthetic insecticide. Nevertheless, ginger oil with various bioactive compounds, such as gingerols and shogaols, possesses antioxidant properties. These compounds are capable of scavenging free radicals and modulate the activity of antioxidative enzymes. Additionally, ginger oil may stimulate the insect's detoxification pathways, leading to the upregulation of antioxidative enzymes and improving its resilience to chemical stressors. The adaptation of P. interpunctella two insecticides may vary and in turn affect redox reaction in the exposed animals.

Conclusions

In conclusion, the comparative study on the insecticidal efficacy of DDVP and ginger root oil on P. interpunctella infesting maize grain provides valuable information for the development of sustainable pest management strategies. The study found that both DDVP and ginger root oil were effective in controlling the infestation of P. interpunctella in maize grain, but the efficacy of DDVP was higher than that of ginger root oil. However, the use of natural insecticides such as ginger root oil could be a viable alternative to synthetic insecticides like DDVP. Also, considering the potential negative impact of synthetic insecticides on human health and the environment, it will be highly recommended if oil extracts of ginger be fortified with little quantity of DDVP in situation were long and lasting insecticidal preservative expected on maize grains infested by P. interpunctella.

Availability of data and material

Data will be made available on request.

Abbreviations

ADPC:

Agricultural Development Programme Centre

CAT:

Catalase

CDNB:

1-Chloro-2, 4-dinitrobenzene

DDVP:

Dichlorvos

GPx:

Glutathione peroxidase

GSH:

Glutathione

GST:

Glutathione transferase

H2O2 :

Hydrogen peroxide

LPO:

Lipid peroxidation

NADPH:

Nicotinamide adenine dinucleotide phosphate

SOD:

Superoxide dismutase

SPSS:

Statistics Package for Social Sciences

USEPA:

United State Environmental Protection Agency

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Acknowledgements

The authors appreciate Ms. Toyin Alade (Technologist in the department of Biology, Federal University of Technology, Akure.) and Dr. Bamidele Olufemi S. (Senior Lecturer, Biochemistry department, Federal University of Technology, Akure) for rendering assistance during the laboratory work.

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Self-sponsored. The authors have received no funding from any organization for the research.

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  1. Department of Biology, School of Life Sciences, Federal University of Technology, P.M.B. 704, Akure, Ondo State, Nigeria

    Folasade Kemisola Olufemi-salami, Joseph Onaolapo Akinneye & Joseph Adewuyi Adeyemi

  2. Department of Food, Science and Technology, Bamidele Olumilua University of Education, Science and Technology, Ikere, Ekiti, Nigeria

    Folasade Kemisola Olufemi-salami

  3. Department of Clinical Analyses, Toxicology and Food Sciences, School of Pharmaceutical Sciences of Ribeirão Preto, University of São Paulo, Avenida do Café s/no, Ribeirão Preto, São Paulo, 14040-903, Brazil

    Joseph Adewuyi Adeyemi

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Olufemi-salami, F.K., Akinneye, J.O. & Adeyemi, J.A. Comparative analysis of active period and oxidative stress of DDVP and ginger (Zingiber officinale) oil on Indian meal moth (Plodia interpunctella Hübner) infesting maize grain. JoBAZ 85, 50 (2024). https://doi.org/10.1186/s41936-024-00377-7

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