Eco-friendly approaches of zinc oxide and silver nitrate nanoparticles along with plant extracts against Spodoptera litura (Fabricius) under laboratory conditions

Abstract

The tobacco cutworm (Spodoptera litura) is a widespread pest that inflicts severe damage on various crops, including cotton, tobacco, and vegetables, with a particular preference for solanaceous plants. Traditional control methods often rely heavily on synthetic insecticides, leading to adverse effects on the environment, human health, and the development of insecticide resistance. In light of these challenges, this study explores the potential of nanotechnology as an innovative and sustainable approach to combat this notorious pest. Bioassays were conducted using laboratory-reared 3rd instar S. litura larvae. Eight different plant extracts coated with zinc oxide and silver nitrate nanoparticles were tested, with concentrations in both distilled water and ethanol at 3, 5, and 7 ml. Data were collected at 24, 48, and 72-h intervals. The results revealed that the highest larval mortality, reaching 98%, was observed in the group treated with silver nitrate nanoparticles derived from Cymbopogon citratus. In comparison, the group treated with zinc oxide nanoparticles dissolved in ethanol exhibited a larval mortality rate of 90%. Ethanol is a polar solvent that is widely used in the synthesis of nanocomposites. It is capable of forming strong hydrogen bonds with oxygen atoms, making it a good dispersant for zinc oxide nanoparticles. Additionally, ethanol has a low boiling point and a non-toxic nature, which makes it a safe and effective option for the dispersion of nanoparticles. Notably, the study concluded that silver nanoparticles combined with ethanol exhibited prolonged and more potent toxic effects against S. litura when compared to zinc oxide nanoparticles. Overall, this research underscores the potential of nanotechnology as a valuable component of Integrated Pest Management (IPM) strategies. By integrating nanotechnology into pest management practices, we can promote sustainable and environmentally friendly approaches that benefit both farmers and the ecosystem.

Keywords

ZnO green NPs

Background

The tobacco cutworm, Spodoptera litura Fabricius (Lepidoptera: Noctuidae) is the most destructive, polyphagous pest of agricultural and horticultural crops^1–3 and extremely infected more than 112 cultivated host plants.⁴ It is widely distributed in Oceania, eastern and southern Asia, north and South America, Australasia, southern and central Africa⁵ including Pakistan.⁶ It is the potential pest of cotton, tobacco, oilseeds, legumes and vegetable crops in Pakistan.¹ It causes massive yield losses in a variety of crops, including soybean 98%,⁷ groundnut 90%,⁸ maize 85%,⁹ cotton 80%,¹⁰ peanuts 70%,¹¹ cabbage 54%¹² and castor 50%.¹³ Male and female adults were identified based on wings, size or color appearance.¹⁴ The female can lay up to 832–923 eggs in a life span^15–17 and larvae of S. litura penetrate in soft tissues like leaf petioles, stems and midribs to feed inside the infected host.¹⁸

Different management strategies are applied to control this destructive pest although chemical control is still commonly used.¹⁹ With the frequent and injudicious application of synthetic insecticides, S. litura has developed resistance against organochlorines, organophosphates, carbamates, pyrethroids^20–25 and new chemistry insecticides.^19,24,25 The application of synthetic insecticides has also adverse impacts on the environment, human health and other living organisms.^26,27 The introduction of genetically modified Bt crops to defend plants against S. litura gained considerable attention at first, however resistance to transgenic crops has also been reported later.^28,29 Biological control presents a sustainable solution to tackle this notorious pest problem. Various biological control agents, such as predators,³⁰ parasitoids,³¹ entomopathogenic nematodes,³² bacteria,³³ fungi^34–36 and nucleopolyhydrousvirus (NPVs),³⁷ are widely employed and its impact on physiological and biochemical activities.

Moreover, nanotechnology is the finest alternative strategy for eradicating these harmful insect pests.^38,39 This nanoscience is inexpensive for farmers and effectively used in sustainable farming.^40,41 Nanoparticles possess unique physical and chemical properties due to their high surface area and nanoscale size. When coated with hazardous chemicals which show completely new properties in comparison to conventional insecticides.^42,43 For the synthesis of nanoparticles different methods are used for instance, biological, physical, and chemical. Toxic substances like plants or plant extracts, enzymes, and microorganisms are covered with various substrates of metals.⁴⁴ These substrates are utilized as a potential safe substitute for conventional chemicals.⁴⁵

Aqueous plant extracts could be coated with nanoparticles of different metals such as zinc oxide, silver nitrate, and gold. Terpeniods and flavanones⁴⁶ which serve as capping and reducing agents as well as being employed to stabilize the NPs, are phytochemicals found in the neem plant extract.⁴⁷ The phytochemicals of Acacia catechu leaf extract include saponins, alkaloids, anthraquinone, flavonoids, triterpenes, tannins and coumarins which stabilize the nanoparticles.⁴⁸

The current research aimed at controlling this notorious pest has been designed by considering the economically important nanotechnology mentioned earlier. This technology offers a more cost-effective solution for farmers while also being environmentally beneficial. The strategy involving silver nitrate and ethanol has demonstrated complete control over S. litura. Nevertheless, to make it commercially viable, additional efforts will be required in the future. These efforts may involve further refining the application methods, optimizing formulations, and conducting larger-scale field trials to ensure its practicality and effectiveness on a broader scale.

Methods

Collection of S. litura

The 4th instar dark green color with yellow and green strips with spots larvae of S. litura⁴⁹ was collected from arum fields by the use of camel hair brush in Head Muhammad Wala (30°11′44.02″N 71°28′31.01″E) Multan, Punjab, Pakistan and shifted in plastic jar 5 × 3 inch and brought into the IPM laboratory of Department of Entomology, Bahauddin Zakariya University (BZU) Multan.

Rearing of S. litura

The larvae of S. litura were reared on the leaves of castor bean (Ricinus communis L.) under laboratory conditions 26 ± 1°C and 60–70% relative humidity with a 14:10 h of light:dark photoperiod.^50,51 Castor bean leaves were collected from the field areas of Northern Bypass Multan (30°6′38.7072″N 71°25′16.1904″E). These leaves were washed 2–3 times with tap water for the removal of contamination, dust and deposition of pathogens and then spread in room for drying. These leaves were provided to the larvae of S. litura as a food source during all instars. Larvae of S. litura were kept separately in plastic jars 5 × 3 inches to prevent cannibalism. The muslin cloth was used to cover the mouth of the plastic jars and tied with a rubber band for proper ventilation and to prevent the larvae from escaping. Castor bean leaves were changed on a daily basis.

After 2 weeks, these larvae secrete the cocoon and enter into pupation and these pupae are shifted into the separate transparent plastic jar 18 × 15 inch. After 1 week, adult emergence takes place. These adults were reared on 10% honey solution. This solution was applied on cotton swabs in a plastic petri dish (5 × 5 cm) as food for adults.^20,52,53 Muslin cloth pieces were hung in rearing jars for egg mass production. Egg batches were collected from the muslin cloth pieces and transferred into a separate plastic jar and after two days hatching took place. Uniform larvae were separated into plastic jars along with a natural diet as castor bean leaves.⁵⁴ Third-instar larvae were used for the experiment. This experiment was conducted under the lab conditions at a temperature of 26 ± 1°C, 60–70% relative humidity, and a light:dark cycle of 14:10 h.⁵⁵

Botanicals extraction

Leaves of Ocimum basilicum L., Syzygium aromaticum L., Jatropha curcas L., Lantana camara L., Eucalyptus globulus L., bulb of Allium sativum L., rhizomes of Zingiber officinale Roscoe and flower buds of Cymbopogon citratus (DC) were collected from field area near BZU, Multan. Leaves of these plant materials were washed two to three times with tap water for the removal of dust and spread into the shaded places for drying for up to 1 week in the laboratory. After drying, these leaves were crushed by the use of an electric grinder and converted into powders. Then these powders were sieved with the use of mash.

For the preparation of plant extracts, 50 ml distilled water along with 5 g powder of each plant were mixed in glass beakers (100 ml). These beakers were tagged which have complete information about botanicals. These beakers were covered with aluminum foil and placed in a water bath and boiled up to 65°C for 2 hours. After heating, beakers were taken out and kept at room temperature for cooling. These plant extract solutions were poured into falcon tubes and centrifuged at 13,000 rpm for 15 min. Then these falcon tubes were removed from the machine and the solution of each plant extract was filtered through Whatman filter paper. Filtered plant extracts are stored at 4°C in a refrigerator.⁵⁶

Preparation of nanoparticles

Nanoparticles were prepared by using four plastic bottles (100 ml) along with two solvents distilled water and ethanol. Two plastic bottles were filled with up to 50 ml of distilled water and the other two glass bottles were filled with up to 50 ml of ethanol. The specified amount of 1 mM zinc oxide solution of 50 ml (0.406 g) was added into two glass bottles one contains distilled water and the other is ethanol. A single plant extract of 5 ml was added to each glass bottle. Glass bottles were covered with aluminum foil sheets to prevent hydrolysis. For the confirmation of NPs synthesis glass bottles were kept in direct sunlight for 3 hours. The color of the solution was changed to whitish in the case of zinc oxide⁵⁷ and dark brown color in the case of silver nitrate.⁵⁸ The same procedure was adopted for silver nitrate (0.849 g). Nanoparticles were stored at 4°C in a refrigerator for further use. The same procedure was followed for all the other botanicals.

Characterization of zinc oxide and silver nitrate nanoparticles

Ultraviolet spectroscopy

Zinc oxide (ZnO) and silver nitrate (AgNO3) nanoparticle synthesis were confirmed by the ultraviolet⁵⁹ visible spectroscopy analysis based on the visual properties. Ultraviolet-Vis spectrophotometer with a wavelength range of 800–200 nm and the spectra were determined at 412 and 296 nm for zinc oxide and silver nitrate nanoparticles, respectively.

EDX and SEM analysis

By smearing a thin layer of an aqueous solution containing zinc oxide and silver nitrate nanoparticles on an aluminum foil sheet, scanning electron microscope pictures were obtained. Smears were detected using Nano-R2TM at a scanning rate (0.5 Hz) and a 20 kV voltage in non-contact mode. For accurate information regarding the composition, crystal structure, and crystalline grain size of nanoparticles X-ray diffraction analysis (XRD), spectrum indicated the synthesis of zinc oxide and silver nitrate nanoparticles, respectively. Analysis was carried out by the Department of Biotechnology Punjab University Lahore, Punjab, Pakistan.

Bioassay

The effectiveness of ZnO and AgNO₃ green nanoparticles was evaluated against the third instar of S. litura larvae by leaf dip method. The castor bean leaves were used as antifeedant. For the bioassay, leaves were washed two to three times with tap water and dried. These leaves were cut into 5 cm by scissors according to the size of plastic petri dishes. Different concentrations such as 3, 5, and 7 mL of zinc oxide and silver nitrate nanoparticles were prepared into falcon tubes. Leaves were dipped into each concentration for 5–10 min and then dried for 2 min. After drying, these leaves were shifted into petri dishes as a food source for larvae. Ten third instar larvae of S. litura were shifted in each plastic petri dish along with the control and each concentration of synthesized nanoparticle was replicated four times. Treated leaves were changed daily (after 24 h). Data were taken after 24, 48, and 72 h and the number of dead larvae was counted. The same procedure was adopted for other synthesized nanoparticles.

Data analysis

Data were analyzed by using statistical software such as SAS (Statistical Analysis System). The SAS software was used for the ANOVA test to compare the means of the findings of the presented data.⁶⁰ Mortality data were analyzed using EPA probit analysis.⁶¹ Mortality was calculated by applying the formula.⁶²

Larval mortality mean (%) = \frac{No . of dead larvae}{No . of exposed larvae} \times 100

Results

Effect of aqueous eight plant extracts synthesized on zinc oxide and silver nitrate nanoparticles using distilled water as a solvent against the mortality of S. litura

The effect of plant extracts synthesized on nanoparticles (containing zinc oxide and silver nitrate in which distilled water was used as solvent) against larval mortality of S. litura is given in Table 1. The highest concentration (7 ml) of both zinc oxide and silver nitrate in O. basilicum nanoparticles caused the highest larval mortality rate of 53% and 60%, respectively, after 72 h. Similarly, nanoparticles of S. aromaticum showed the highest larval mortality 55% with zinc oxide and 63% with silver nitrate at the highest concentration (7 ml) after 72 h. Maximum larval mortality of 60% with zinc oxide and 65% with silver nitrate after 72 h at the highest concentration (7 ml) was observed in J. curcas nanoparticles. L. camara nanoparticles with zinc oxide showed maximum larval mortality of 60% but 70% with silver nitrate at the highest concentration (7 ml) after 72 h. Likewise, the maximum larval mortality after the application of A. sativum nanoparticles was 58% with zinc oxide and 70% with silver nitrate at the highest concentration (7 ml) after 72 h. The maximum larval mortality rates at the highest concentration (7 ml) were 58 and 80% when treated with zinc oxide and silver nitrate E. globulus nanoparticles, respectively after 72 h. Z. officinale nanoparticles coated with zinc oxide exhibited the highest larval mortality of 73%, compared to silver nitrate which caused 85% at the highest concentration (7 ml) after 72 h. However, as compared to all above-mentioned nanoparticles, the maximum larval mortality of 83% in the case of C. citratus nanoparticles with zinc oxide and 95% with silver nitrate at the highest concentration (7 ml) was observed after 72 h against larvae of S. litura. Similar trends were observed for all green nanoparticles at 24 and 48 h against S. litura larvae (Table 1). The results demonstrate that an increase in the concentration of nanoparticles increased larval mortality.

Table 1.

Larvicidal activity of plant extracts at different concentrations coated on zinc oxide and silver nitrate nanoparticles dissolved in distilled water against S. litura larvae.

Mortality % (± S.D)
Plant extracts	Con. plant extracts on NPs (ml)	Zinc oxide dissolved in distilled water			Silver nitrate
Plant extracts	Con. plant extracts on NPs (ml)	24h	48h	72h	24h	48h	72h
O. basilicum	3	3 (±5.00)	5 (±10.0)	15 (±5.77)	5 (±5.77)	10 (±0.00)	18 (±5.00)
	5	8 (±5.00)	18 (±5.00)	23 (±12.5)	10 (±8.16)	23 (±5.00)	33 (±5.00)
	7	15 (±5.77)	51 (±5.00)	53 (±5.77)	20 (±8.16)	53 (±5.00)	60 (±8.16)
S. aromaticum	3	5 (±5.77)	10 (±0.00)	23 (±5.00)	10 (±0.00)	15 (±5.77)	28 (±12.5)
	5	10 (±11.6)	20 (±8.16)	28 (±9.57)	15 (±5.77)	28 (±5.00)	35 (±5.77)
	7	20 (±8.16)	53 (±12.5)	55 (±12.9)	35 (±10.0)	55 (±5.77)	63 (±5.00)
J. curcas	3	5 (±5.77)	15 (±5.77)	23 (±5.00)	15 (±5.77)	25 (±5.77)	33 (±5.00)
	5	15 (±10.0)	23 (±5.00)	35 (±10.0)	25 (±5.77)	30 (±8.16)	45 (±5.77)
	7	28 (±9.57)	53 (±5.00)	60 (±11.5)	35 (±5.77)	58 (±5.00)	65 (±5.77)
L. camara	3	13 (±12.6)	18 (±5.00)	25 (±5.77)	18 (±5.00)	25 (±5.77)	35 (±5.77)
	5	18 (±9.57)	30 (±8.16)	38 (±5.00)	25 (±5.77)	40 (±8.16)	50 (±8.16)
	7	30 (±8.16)	55 (±5.77)	60 (±8.16)	43 (±12.5)	63 (±12.5)	70 (±8.16)
A. sativum	3	18 (±5.00)	25 (±12.9)	33 (±9.57)	25 (±5.77)	35 (±5.77)	40 (±8.16)
	5	23 (±5.00)	35 (±12.9)	45 (±10.0)	33 (±9.57)	45 (±5.77)	55 (±5.77)
	7	33 (±5.00)	53 (±15.0)	58 (±9.57)	45 (±5.77)	63 (±5.00)	70 (±8.16)
E. globulus	3	15 (±5.77)	25 (±5.77)	33 (±5.00)	25 (±10.0)	35 (±5.77)	40 (±8.16)
	5	25 (±5.77)	40 (±8.16)	48 (±5.00)	35 (±5.77)	50 (±8.16)	63 (±15.0)
	7	38 (±5.00)	53 (±9.57)	58 (±12.5)	43 (±5.00)	68 (±9.57)	80 (±8.16)
Z. officinale	3	23 (±5.00)	30 (±8.16)	40 (±8.16)	33 (±5.00)	40 (±8.16)	45 (±12.9)
	5	33 (±5.00)	48 (±5.00)	58 (±9.57)	43 (±5.00)	58 (±15.0)	68 (±5.00)
	7	43 (±5.00)	60 (±8.16)	73 (±9.57)	55 (±12.9)	73 (±9.57)	85 (±5.77)
C. citratus	3	23 (±5.00)	35 (±10.0)	40 (±8.16)	30 (±8.16)	40 (±8.16)	45 (±5.77)
	5	35 (±5.77)	55 (±12.9)	65 (±5.77)	48 (±9.57)	68 (±5.00)	78 (±15.0)
	7	48 (±5.00)	70 (±11.5)	83 (±9.57)	65 (±10.0)	83 (±15.0)	95 (±5.77)

Conc. : Concentration.

Effect of aqueous eight plant extracts synthesized on zinc oxide and silver nitrate nanoparticles using ethanol as a solvent against the mortality of S. litura

Effect of plant extracts synthesized on nanoparticles (containing zinc oxide and silver nitrate in which ethanol was used as solvent) against larval mortality of S. litura is given in Table 2. O. basilicum nanoparticles at the highest concentration (7 ml) with zinc oxide showed a maximum larval mortality of 58%, compared to 65% in the case of silver nitrate after 72 h of treatment against S. litura larvae. Similarly, S. aromaticum nanoparticles at the highest concentration (7 ml) showed the highest mortality 60% with zinc oxide and 68% with silver nitrate after 72 h. Maximum larval mortality recorded at the highest concentration (7 ml) of J. curcas nanoparticles with zinc oxide was 63% and with silver nitrate was 70% after 72 h. Larvae of S. litura exhibited a maximum mortality of 65% when exposed to L. camara nanoparticles combined with zinc oxide as compared to silver nitrate which caused 83% mortality at the highest concentration (7 ml) after 72 h. Likewise, the maximum larval mortality at the highest concentration (7 ml) by A. sativum nanoparticles was 63% with zinc oxide and 80% with silver nitrate evaluated after 72 h. The highest larval mortality rates with zinc oxide and silver nitrate were 68% and 95%, respectively observed after 72 h in E. globulus nanoparticles at the highest concentration (7 ml). Z. officinale nanoparticles at a maximum concentration (7 ml) coated with zinc oxide exhibited the highest mortality 78%, compared to silver nitrate which caused 97% at the highest concentration (7 ml) after 72 h. In contrast to other synthesized nanoparticles, C. citratus nanoparticles caused maximum larval mortality of 90% at the highest concentration (7 ml) with zinc oxide as compared to silver nitrate which caused the highest larval mortality of 98% after 72 h. All nanoparticles exhibited the same trend of larval mortality with an increase in concentration after 24 and 72 h of exposure (Table 2).

Table 2.

Larvicidal activity of plant extracts at different concentrations coated on zinc oxide and silver nitrate nanoparticles dissolved in ethanol against S. litura larvae.

Mortality % (± S.D)
Plant extracts	Conc. of plant extracts on NPs (ml)	Zinc oxide Dissolved in ethanol			Silver nitrate
Plant extracts	Conc. of plant extracts on NPs (ml)	24h	48h	72h	24h	48h	72h
O. basilicum	3	8 (±5.00)	13 (±5.00)	25 (±17.3)	13 (±9.57)	15 (±12.9)	23 (±9.57)
	5	13 (±9.57)	20 (±14.1)	33 (±15.0)	20 (±8.16)	25 (±12.9)	35 (±5.77)
	7	20 (±0.00)	55 (±5.77)	58 (±5.00)	30 (±8.16)	58 (±5.00)	65 (±5.77)
S. aromaticum	3	8 (±9.57)	13 (±5.00)	25 (±12.9)	15 (±5.77)	23 (±9.57)	33 (±9.57)
	5	13 (±5.00)	23 (±5.00)	33 (±5.00)	23 (±9.57)	35 (±10.0)	43 (±5.00)
	7	25 (±5.77)	55 (±5.77)	60 (±8.16)	40 (±8.16)	63 (±5.00)	68 (±12.5)
J. curcas	3	8 (±5.00)	20 (±8.16)	28 (±9.57)	23 (±5.00)	30 (±8.16)	38 (±9.57)
	5	20 (±8.16)	28 (±9.57)	40 (±8.16)	33 (±5.00)	38 (±9.57)	50 (±8.16)
	7	30 (±8.16)	55 (±5.77)	63 (±12.5)	45 (±10.0)	63 (±9.57)	70 (±8.16)
L. camara	3	15 (±5.77)	23 (±5.00)	30 (±8.16)	23 (±5.00)	30 (±8.16)	43 (±5.00)
	5	20 (±8.16)	35 (±5.77)	43 (±5.00)	33 (±5.00)	45 (±10.0)	58 (±15.0)
	7	38 (±5.00)	58 (±12.5)	65 (±5.77)	53 (±9.57)	70 (±8.16)	83 (±9.57)
A. sativum	3	23 (±5.00)	30 (±8.16)	38 (±5.00)	33 (±9.57)	40 (±0.00)	45 (±5.77)
	5	28 (±5.00)	43 (±9.57)	50 (±8.16)	40 (±8.16)	55 (±12.9)	65 (±5.77)
	7	40 (±8.16)	58 (±9.57)	63 (±9.57)	53 (±9.57)	73 (±5.00)	80 (±8.16)
E. globulus	3	23 (±5.00)	30 (±8.16)	38 (±9.57)	35 (±5.77)	43 (±5.00)	48 (±9.57)
	5	30 (±8.16)	43 (±9.57)	55 (±12.9)	55 (±5.77)	65 (±5.77)	75 (±5.77)
	7	40 (±8.16)	63 (±9.57)	68 (±5.00)	75 (±10.0)	88 (±9.57)	95 (±5.77)
Z. officinale	3	28 (±5.00)	38 (±9.57)	43 (±5.00)	38 (±5.00)	43 (±5.00)	48 (±12.6)
	5	38 (±5.00)	53 (±9.57)	63 (±5.00)	50 (±8.16)	65 (±10.0)	78 (±9.57)
	7	48 (±5.00)	65 (±5.77)	78 (±5.00)	60 (±8.16)	83 (±5.00)	97 (±5.00)
C. citratus	3	28 (±5.00)	38 (±17.0)	43 (±5.00)	38 (±9.57)	43 (±5.00)	48 (±5.00)
	5	43 (±5.00)	60 (±8.16)	73 (±5.00)	60 (±8.16)	70 (±10.0)	83 (±9.57)
	7	55 (±5.77)	75 (±12.9)	90 (±0.00)	75 (±5.77)	88 (±5.00)	98 (±5.00)

Discussion

S. litura, recognized as the cotton leafworm or tobacco cutworm, holds significance as a major agricultural crop pest.^11,20 Its significance is due to the damage to a variety of crops, which can lead to substantial economic losses for farmers and the agricultural industry.⁶³ The larvae of S. litura consume plant tissues with great appetite, leading to defoliation, stunting and complete crop destruction.¹ This ultimately results in reduced yields and significant economic hardships for farmers.¹⁸ Farmers commonly employ a range of tactics to handle the impact of S. litura, including the use of chemical insecticides, biological control agents and genetically modified crops with built-in insect resistance.¹⁹ These strategies aim to effectively manage and minimize the harm caused by this pest.⁶⁴ Implementing these control approaches can lead to significant additional costs in the production process. From a broader perspective, the economic importance of S. litura stems from its capacity to inflict substantial damage on crops, necessitating substantial financial commitments toward preventive measures and research. This is crucial for upholding sustainable agriculture and ensuring food security.

The present research assessed the insecticidal impacts of zinc oxide and silver nitrate when combined with eight different plant extracts. The goal was to determine their effectiveness in reducing the survival of S. litura larvae. Among these, the nanoparticles derived from C. citratus, in conjunction with silver nitrate and ethanol, exhibited the highest mortality rates. Following closely, nanoparticles from Z. officinale also demonstrated significant effectiveness against S. litura larvae. Previously, traditional insecticides have been employed to combat S. litura and various other insect pests.^19,65 However, excessive use of insecticides leads to the development of insect resistance.^20,23,25,66 Additionally, the long-term ecological impacts of nanoparticle application on non-target species and the environment remain uncertain and require further investigation. Furthermore, while the study focused on a specific pest and nanoparticle combination, generalizing these findings to diverse pest-crop systems and various nanoparticle formulations may not be straightforward. These limitations underscore the need for continued research and a cautious approach to applying nanoparticle-based pest control methods in practical agriculture. Nanoparticles have displayed noteworthy toxicity toward diverse insect pests.^38,41

The process of extracting and utilizing nanoparticles that are synthesized from plants presents a promising avenue of research for pest control. Plant extracts serve as highly effective biological precursors for the synthesis of nanoparticles such as zinc, silver, iron and gold, showcasing their potential significance in this field.³⁵ Due to their shape and size, these synthesized nanoparticles are simple to use on plants.^36,67 Nanoparticles synthesized with green material have been used in various aspects including pest control due to safer usage for people and the environment. In recent research, different techniques were used to evaluate the synthesis of zinc oxide and silver nitrate nanoparticles using eight plant extracts. These nanoparticles of zinc oxide and silver nitrate were applied to S. litura to evaluate the effects of nanoparticles on the mortality of experimental species.

Employing nanoparticles synthesized through environmentally friendly methods diminishes the negative impact of pesticides on the environment. This approach also facilitates the creation of ecologically sound alternatives for pest control, including safer pesticides, insecticides, and repellents targeted toward insect pests. Similarly to the results leaf extract (H. tiliaceus) coated on silver nitrate AgNO₃ solution was reported as the highest anti-feeder (94%) against third instar larvae of S. litura at 200 g of Ag NPs.⁶⁸ Similar to the results Z. officinale leaf extract coated on ZnO nanoparticles showed 100% mortality against 3^rd third instar larvae of S. litura was recorded at a concentration of 500 ppm.⁶⁹ Likewise to the findings leaf extract of C. citratus coated on gold nanoparticles was reported as the most toxic (99%) against 1st instar larvae of Anopheles stephensi while (93%) in the case of A. aegypti at a concentration of 500 ppm.⁷⁰ Consistent with the findings, the most substantial mortality rate of 100% was observed in the first and second instar larvae of C. quinquefasciatus when exposed to biosynthesized gold nanoparticles derived from C. citratus plant extract, at a concentration of 3.2 ppm. Likewise, a mortality rate of 100% was recorded in the first instar larvae of Anthocepholus cadamba treated with methanolic extracts of C. citratus, at a concentration of 80 ppm. Phytochemicals like terpenoids and flavanones are abundant in C. citratus leaf extract. Those phytochemical ingredients act directly as reducing agents.⁷¹ Likewise to the findings in aqueous soya-based Ag NPs extract, 100% mortality was recorded against third instar larvae of S. litura.⁴⁰ Similar to the findings, 91% mortality was observed in NPs of ZnO at 5% concentration.⁷² Similar to the findings ethanolic extract of Chrysanthemum coated on silver nitrate nanoparticles was reported as the highest anti-feeder (96%) at a concentration of 36 ppm against fourth instar larvae of A. aegypti.⁷³ In the current investigation, the mortality of pests exhibited an upward trend in correlation with an escalation in the concentration of nanoparticles. By employing nanoparticles synthesized through environmentally friendly methods, we contribute to mitigating the adverse environmental effects associated with traditional pesticides. This approach not only paves the way for ecologically sound alternatives in pest control but also holds promise for the development of safer pesticides, insecticides, and repellents. A similar finding was proposed by Devi et al.⁷⁴ who observed a direct relation between the concentration of NPs with mortality of H. armigera.

Conclusion

In this study, we have explored the use of plant extracts, particularly Cymbopogon citratus (lemongrass), for the eco-friendly synthesis of nanoparticles as a means of effectively managing Spodoptera litura (tobacco cutworm). These plant extracts, known for their renewability and environmental friendliness, serve as excellent reducing agents for nanoparticle synthesis. Notably, silver nanoparticles synthesized from C. citratus leaf extract exhibited significantly higher toxicity against S. litura larvae when compared to zinc oxide nanoparticles. Our findings strongly advocate for the adoption of biological techniques in nanoparticle synthesis, thereby eliminating the need for toxic and hazardous solvents. The eco-friendly nature of these nanoparticles, especially C. citratus silver nanoparticles, suggests their safe application in S. litura management, potentially in combination with other environmentally safe methods. Furthermore, this research presents a compelling case for future investigations into the large-scale utilization of green nanoparticles for the control of major lepidopteran pests. This approach aligns seamlessly with the principles of sustainable agriculture and environmentally conscious pest management, offering a promising avenue for the agricultural industry's future. In conclusion, this study underscores the potential of green nanoparticles to revolutionize sustainable pest control practices, providing an innovative and environmentally friendly solution to the challenges posed by agricultural pests like S. litura.

Footnotes

Acknowledgements

We thank Professor Hour Youmimg for critically reviewed this manuscript and gave some valuable suggestions.

Authors’ contributions

All authors equally contributed in the manuscript.

Availability of data and material

Data will available on request.

Consent for publication

All authors are well aware and agree to submit manuscript.

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: We are thankful to the Higher Education Commission, Pakistan for financial support.

ORCID iD

Habib Ali

Author biographies

Aqsa Shabir is a dedicated PhD scholar in the Department of Entomology at Bahauddin Zakariya University in Multan, Punjab, Pakistan. Her academic journey has been marked by a profound interest in insect diversity and abundance, leading to significant contributions in the field. Throughout her scholarly pursuits, she has undertaken substantial research focused on understanding the intricacies of insect diversity and abundance. Her work reflects a keen curiosity about the natural world and a commitment to unraveling the complexities of entomology. Her academic achievements extend beyond the laboratory, as she has made noteworthy contributions through the publication of various research papers. Her written works not only showcase her expertise in the subject matter but also contribute valuable insights to the broader scientific community. In addition to her written contributions, she has actively participated in academic conferences, where she has had the opportunity to present her research findings. Through these presentations, she has shared her knowledge with peers, fostering discussions and collaborations that further enrich the field of entomology. As a PhD scholar, her journey is characterized by a passion for exploration, a dedication to academic excellence, and a commitment to advancing our understanding of insect diversity. Her work stands as a testament to her contributions to the academic community and her commitment to the ongoing exploration of the fascinating world of entomology.

Zahid Mahmood Sarwar is a dedicated academic and researcher currently serving in the Department of Entomology at Bahauddin Zakariya University in Multan, Punjab, Pakistan. His professional journey has been characterized by an unwavering passion for teaching and research, with a focus on arthropod biodiversity, acarology, and insect taxonomy. His commitment to continuous learning and skill enhancement is evident in his dedication to staying abreast of the latest trends and technologies in his research areas. Driven by a deep-seated belief in the power of innovation, he actively seeks to leverage technology to expand the boundaries of what can be achieved in his field. His ultimate career aspiration is to lead a research and development team, where he envisions spearheading the creation of groundbreaking solutions and new product ideas. With an impressive scholarly record, he has published nearly 40 articles in highly impactful journals. Additionally, he has authored one book and supervised 18 M.Sc. and 2 PhD thesis research projects. As a committee member, he has contributed to the guidance of 4 MSc and MPhil research theses. His journey reflects not only his academic prowess but also his commitment to pushing the boundaries of knowledge and inspiring positive change in the field of entomology.

Habib Ali (PhD in Agricultural Entomology and Insect Pest Control), currently serving as a dedicated faculty member at Khwaja Fareed University of Engineering and Information Technology, located in Rahim Yar Khan, Pakistan. His academic journey began in September 2012 when he graduated from the University of Agriculture Faisalabad, Pakistan, specializing in Agricultural Entomology. In December 2018, he successfully earned his PhD from Fujian Agriculture and Forestry University (FAFU) in Fujian, China. He is a fervent researcher with an impressive track record of contributions to the scientific community. He has authored numerous research papers, both nationally and internationally, in high-impact journals. His collective impact factor from these publications is approximately 300. Notable journals that have featured his work include “Frontiers in Microbiology,” “Molecular Phylogenetics and Evolution,” “Insects,” “Journal of Economic Entomology,” and “Microbial Pathogenesis.” Furthermore, he has authored eight book chapters. He is also an accomplished author and editor, having published books with respected publishers such as Springer, Taylor and Francis, IntechOpen, and Elsevier. His contributions to the field have been acknowledged with several prestigious awards, including the Best International Student of the Year and the Best Thesis Award from the China Scholarship Council (CSC). In addition, he was nominated for the World Scientist Index in 2021 and received the Council of Asian Science Editorship. In addition to his research and academic achievements, he has actively participated in various international conferences, symposiums, and workshops. He has undertaken educational and faculty training programs and has contributed to both national and international research projects. Furthermore, he generously dedicates his time as an editor and reviewer for national and international journals. His research interests encompass a wide range of topics within the field of agricultural entomology, molecular entomology, microbial pathogenesis, bee health and disease management, crop pests, biological control of pests.

References

Ahmad

Ghaffar

Rafiq

. Host plants of leaf worm, Spodoptera litura (Fabricius)(Lepidoptera: noctuidae) in Pakistan. Asian J Agric Biol 2013; 1: 23–28.

Ramzan

Ilahi

Umar

, et al. Biological parameters of Armyworm, Spodoptera litura and toxicity of three insecticides against 3rd instars larvae under laboratory conditions. Indian J Pure Appl Biosci 2021; 9: 12–17.

Arumugam

Muthusamy

Dhamodaran

, et al. Pesticidal activity of Rivina humilis L. (Phytolaccaceae) against important agricultural polyphagous field pest, Spodoptera litura (Fab.)(Lepidoptera: noctuidae). J Coast Life Med 2015; 3: 389–394.

Xie

, et al. Functional analysis of SlGSTE12 in pyrethroid and organophosphate resistance in Spodoptera litura. J Agric Food Chem 2021; 69: 5840–5848.

Yoon

Lee

W-H

. Methodological analysis of bioclimatic variable selection in species distribution modeling with application to agricultural pests (Metcalfa pruinosa and Spodoptera litura). Comput Electron Agric 2021; 190: 106430.

Mahmoon

Ali

, et al. Bionomics and management of aphid, Brevicoryne brassicae (Homoptera: aphididae) on canola (Brassica napus) using Chrysoperla carnea. J Trop Insect Sci 2022; 42: 3327–3333.

Fattah

Sjam

Diana Daud

, et al. Impact of armyworm Spodoptera litura (Lepidoptera: noctuidae) attack: damage and loss of yield of three soybean varieties in South Sulawesi. Indonesia J Crop Prot 2020; 9: 483–495.

War

Paulraj

War

, et al. Herbivore-and elicitor-induced resistance in groundnut to Asian armyworm, Spodoptera litura (Fab.)(Lepidoptera: noctuidae). Plant Signal Behav 2011; 6: 1769–1777.

Nawaz

Ali

Fiaz

, et al. Analysis of food resources, host availability and insecticidal impacts on the fecundity, longevity and parasitism efficiency of Diaertiella rapae (M’intosh). Int J Trop Insect Sci 2021; 41: 2883–2896.

10.

Maqsood

Sabri

Ali

, et al. Comparative toxicity of some insecticides against army worm, Spodoptera litura L.(Lepidoptera: noctuidae) under laboratory conditions. J Entomol Zool Stud 2016; 5: 770–773.

11.

Tuan

Lee

Chi

. Population and damage projection of Spodoptera litura (F.) on peanuts (Arachis hypogaea L.) under different conditions using the age stage, two sex life table. Pest Manag Sci 2014; 70: 805–813.

12.

Sahu

Pachori

Navya

, et al. Extent of damage by Spodoptera litura on cabbage. J Entomol Zool Stud 2020; 8: 1153–1156.

13.

Muddanuru

Polumetla

Maddukuri

, et al. Development and evaluation of transgenic castor (Ricinus communis L.) expressing the insecticidal protein Cry1Aa of Bacillus thuringiensis against lepidopteran insect pests. J Crop Prot 2019; 119: 113–125.

14.

. 7/124 (1) Spodoptera littoralis, Spodoptera litura, Spodoptera frugiperda, Spodoptera eridania. EPPO Bull 2015; 45: 410–444.

15.

Gopika

Sonkamble

Lad

. Biology and morphometry of tobacco leaf eating caterpillar, Spodoptera litura on cabbage (Brassica olearacea var. capitata L.). J Pharm Innov 2021; 10: 1568–1571.

16.

Zhao

Xie

, et al. Seasonal pattern of Spodoptera litura (Lepidoptera: noctuidae) migration across the Bohai Strait in northern China. J Econ Entomol 2015; 108: 525–538.

17.

Xue

, et al. Laboratory evaluation of flight activity of the common cutworm, Spodoptera litura (Lepidoptera: noctuidae). Insect Sci 2010; 17: 53–59.

18.

Sarwar

. Some insect pests (Arthropoda: insecta) of summer vegetables, their identification, occurrence, damage and adoption of management practices. Int J Sustain Agric 2014; 1: 108–117.

19.

Ahmad

Butt

Idrees

, et al. Toxicity of four new chemistry insecticides against Spodoptera litura (noctuidae: lepidoptera) under controlled laboratory conditions. J B M 2022; 9: 5.

20.

Ahmad

Arif

Ahmad

. Occurrence of insecticide resistance in field populations of Spodoptera litura (Lepidoptera: noctuidae) in Pakistan. J Crop Prot 2007; 26: 809–817.

21.

Armes

Wightman

Jadhav

, et al. Status of insecticide resistance in Spodoptera litura in Andhra Pradesh. India Pestic Sci 1997; 50: 240–248.

22.

Kim

Y-G

Cho

J-R

Lee

J-I

, et al. Insecticide resistance in the tobacco cutworm, Spodoptera litura (Fabricius)(Lepidoptera: noctuidae). J Asia Pac Entomol 1998; 1: 115–122.

23.

Saleem

Ahmad

, et al. Resistance to selected organochlorin, organophosphate, carbamate and pyrethroid, in Spodoptera litura (Lepidoptera: noctuidae) from Pakistan. J Econ Entomol 2008; 101: 1667–1675.

24.

Shad

Sayyed

Fazal

, et al. Field evolved resistance to carbamates, organophosphates, pyrethroids, and new chemistry insecticides in Spodoptera litura fab.(lepidoptera: noctuidae). J Pest Sci 2012; 85: 153–162.

25.

Tong

Zhou

, et al. Field resistance of Spodoptera litura (Lepidoptera: noctuidae) to organophosphates, pyrethroids, carbamates and four newer chemistry insecticides in Hunan, China. J Insect Sci 2013; 86: 599–609.

26.

Memon

QUA

Wagan

Chunyu

, et al. Health problems from pesticide exposure and personal protective measures among women cotton workers in southern Pakistan. Sci Total Environ 2019; 685: 659–666.

27.

Ahmad

Shahid

Khalid

, et al. Residues of endosulfan in cotton growing area of Vehari, Pakistan: an assessment of knowledge and awareness of pesticide use and health risks. Environ Sci Pollut Res 2019; 26: 20079–20091.

28.

Wan

Huang

, et al. Population dynamics of Spodoptera litura (Lepidoptera: noctuidae) on Bt cotton in the Yangtze River valley of China. Environ Entomol 2008; 37: 1043–1048.

29.

Yinghua

Yan

Jin

, et al. Responses of the cutworm Spodoptera litura (Lepidoptera: noctuidae) to two Bt corn hybrids expressing Cry1Ab. Sci Rep 2017; 7: 1–13.

30.

Y-Y

Wang

Y-N

Zhang

H-Z

, et al. The green lacewing Chrysopa formosa as a potential biocontrol agent for managing Spodoptera frugiperda and Spodoptera litura. Bull Entomol Res 2023; 113: 49–62.

31.

Nawaz

Ali

Sufyan

, et al. In-vitro assessment of food consumption, utilization indices and losses promises of leafworm, Spodoptera litura (Fab.), on okra crop. Asia Pac Entomol 2020; 23: 60–66.

32.

Tomar

Thakur

. Biocidal potential of indigenous isolates of Entomopathogenic Nematodes (EPNs) against tobacco cutworm, Spodoptera litura Fabricius (lepidoptera: noctuidae). Egypt J Biol Pest Control 2022; 32: 1–10.

33.

Ali

Muhammad

Sanda

, et al. Pyrosequencing uncovers a shift in bacterial communities across life stages of Octodonta nipae (Coleoptera: chrysomelidae). Front Microbiol 2019; 10: 466.

34.

Islam

SMN

Chowdhury

MZH

Mim

, et al. Biocontrol potential of native isolates of Beauveria bassiana against cotton leafworm Spodoptera litura (Fabricius). Sci Rep 2023; 13: 8331.

35.

Rasheed

Bilal

Iqbal

, et al. Green biosynthesis of silver nanoparticles using leaves extract of Artemisia vulgaris and their potential biomedical applications. Colloids surf. B Biointerfaces 2017; 158: 408–415.

36.

Kumar

Yadav

. Plant mediated synthesis of silver and gold nanoparticles and their applications. J Chem Technol Biotechnol 2009; 84: 151–157.

37.

Sarwar

Maan

Ayub

, et al. Evaluation of indigenous the nucleopolyhedrovirus (NPV) of Spodoptera litura (Fabricius)(Lepidoptera: noctuidae) in combination with chlorantraniliprole against Spodoptera species. Egypt J Biol Pest Cont 2021; 31: 1–7.

38.

Jafir

Ahmad

Arif

, et al. Characterization of Ocimum basilicum synthesized silver nanoparticles and its relative toxicity to some insecticides against tobacco cutworm, Spodoptera litura Feb.(Lepidoptera; Noctuidae). Ecotoxicol Environ Saf 2021; 218: 112278.

39.

Kalaimurugan

Vivekanandhan

Sivasankar

, et al. Larvicidal activity of silver nanoparticles synthesized by Pseudomonas fluorescens YPS3 isolated from the Eastern Ghats of India. J Clust Sci 2019; 30: 225–233.

40.

Hosamani

Patil

Benagi

, et al. Synthesis of green silver nanoparticles from soybean seed and its bioefficacy on Spodoptera litura (F.). Int J Curr Microbiol Appl Sci 2019; 8: 610–618.

41.

Singh

Handa

Manchanda

. Nanoparticles in sustainable agriculture: an emerging opportunity. J Control Release 2021; 329: 1234–1248.

42.

Willems

. Roadmap report on nanoparticles. Barcelona, Spain: W&W Espana sl, 2005, 157.

43.

Rahman

Pittarate

Perumal

, et al. Larvicidal and antifeedant effects of copper nano-pesticides against Spodoptera frugiperda (JE Smith) and its immunological response. Insects 2022; 13: 1030.

44.

Vivekanandhan

Swathy

Thomas

, et al. Insecticidal efficacy of microbial-mediated synthesized copper nano-pesticide against insect pests and non-target organisms. Int J Environ Res Public Health Int J Env Res Pub He 2021; 18: 10536.

45.

Mohanpuria

Rana

Yadav

. Biosynthesis of nanoparticles: technological concepts and future applications. J Nanoparticle Res 2008; 10: 507–517.

46.

Ujah

Nsude

Ani

, et al. Phytochemicals of neem plant (Azadirachta indica) explains its use in traditional medicine and pest control. GSC Biol Pharm Sci 2021; 14: 165–171.

47.

Verma

Mehata

. Controllable synthesis of silver nanoparticles using Neem leaves and their antimicrobial activity. J Radiat Res Appl Sci 2016; 9: 109–115.

48.

Baranitharan

Alarifi

Alkahtani

, et al. Phytochemical analysis and fabrication of silver nanoparticles using Acacia catechu: an efficacious and ecofriendly control tool against selected polyphagous insect pests. Saudi J Biol Sci 2021; 28: 148–156.

49.

Latha

Shivanna

Manjunatha

, et al. Biology of Spodoptera litura on chewing tobacco in vitro. J Eco-Friendly Agric 2014; 9: 43–47.

50.

Arivoli

Tennyson

. Antifeedant activity, developmental indices and morphogenetic variations of plant extracts against Spodoptera litura (Fab)(Lepidoptera: noctuidae). J Entomol Zoo. Stud 2013; 1: 87–96.

51.

Supriya

Dash

Ingole

, et al. Natural parasitization of Cotesia spp. and Bracon spp. on Spodoptera litura Fab. in castor crop. J Pharm Innov 2022; 12: 2875–2877.

52.

Indhumathi

Arivudainambi

. Biological activities of certain plant extracts against Tobacco caterpillar Spodoptera litura Fab. Plant Arch 2019; 19: 2872–2876.

53.

Zakria

Zaib

Abbas

, et al. Influence of temperature on the development and reproduction of Spodoptera litura (Fabricius) on castor bean: implications for its use as a trap crop. Arthropod-Plant Interact 2022; 16: 505–515.

54.

Ramaiah

Maheswari

. Biology studies of tobacco caterpillar, Spodoptera litura Fabricius. J Entomol Zool Stud 2018; 6: 2284–2289.

55.

Saljoqi

A-U-R

Khan

Ali

. Rearing of Spodoptera litura (Fabricius) on different artificial diets and its parasitization with Trichogramma chilonis (Ishii). Pak J Zool 2015; 47: 169–175.

56.

Espenti

Rao

. Bio-synthesis and characterization of silver nanoparticles using Terminalia chebula leaf extract and evaluation of its antimicrobial potential. Mater Lett 2016; 174: 129–133.

57.

Ogunyemi

Abdallah

Zhang

, et al. Green synthesis of zinc oxide nanoparticles using different plant extracts and their antibacterial activity against Xanthomonas oryzae pv. oryzae. Artif. Cells nanomed. Biotechnol 2019; 47: 341–352.

58.

Aritonang

Kojong

Koleangan

, et al. Green synthesis of silver nanoparticles using Lantana camara fresh leaf extract for qualitative detection of Hg 2+, Cu 2+, Pb 2+, and Mn 2 + in aqueous solution. Indones J Chem 2021; 21: 990–1002.

59.

Bhattacharyya

Bhaumik

Rani

, et al. Nano-particles—A recent approach to insect pest control. Afr J Biotechnol 2010; 9: 3489–3493.

60.

Ali

Muhammad

Bala

, et al. Genomic evaluations of Wolbachia and mtDNA in the population of coconut hispine beetle, Brontispa longissima (Coleoptera: chrysomelidae). Mol Phylogenet Evol 2018; 127: 1000–1009.

61.

Ali

Muhammad

, et al. The endosymbiotic Wolbachia and host COI gene enables to distinguish between two invasive palm pests; coconut leaf beetle, Brontispa longissima and hispid leaf beetle, Octodonta nipae. J Econ Entomol 2018; 111: 2894–2902.

62.

Asghar

Sarwar

Almadiy

, et al. Toxicological effects of silver and zinc oxide nanoparticles on the biological and life table parameters of Helicoverpa armigera (Noctuidae: lepidoptera). Agric 2022; 12: 1744.

63.

Bragard

Dehnen-Schmutz

Di Serio

, et al. Pest categorisation of Spodoptera litura. Efsa J 2019; 17: e05765.

64.

Srivastava

Sharma

Anal

, et al. Integrated management of Spodoptera litura: a review. Int J Life Sci Scienti Res 2018; 4: 1536–1538.

65.

Bhatti

Ahmad

Yousaf

, et al. Pyrethroids and new chemistry insecticides mixtures against Spodoptera litura (Noctuidae: lepidoptera) under laboratory conditions. Asian J Agric Biol 2013; 1: 45–50.

66.

Kranthi

Jadhav

Kranthi

, et al. Insecticide resistance in five major insect pests of cotton in India. Crop Prot 2002; 21: 449–460.

67.

Nawaz

Ali

Sufyan

, , et al. Comparative bio-efficacy of nuclear polyhedrosis virus (NPV) and Spinosad against American bollwormm, Helicoverpa armigera (hubner). Rev Bras Entomol 2020; 63: 277–282.

68.

Rani

Laxmi

Vadlapudi

, et al. Phytofabrication of silver nanoparticles using the mangrove associate, Hibiscus tiliaceus plant and its biological activity against certain insect and microbial pests. J Biopestic 2016; 9: 167.

69.

Thakur

Kumari

, et al. Nano-insecticide: synthesis, characterization, and evaluation of insecticidal activity of ZnO NPs against Spodoptera litura and Macrosiphum euphorbiae. Appl Nanosci 2022; 12: 3835–3850.

70.

Murugan

Benelli

Panneerselvam

, et al. Cymbopogon citratus-synthesized gold nanoparticles boost the predation efficiency of copepod Mesocyclops aspericornis against malaria and dengue mosquitoes. Exp Parasitol 2015; 153: 129–138.

71.

Jeyalalitha

Murugan

Madhiyazhagan

. Bioefficacy of plant-mediated gold nanoparticles and Anthocepholus cadamba on filarial vector, Culex quinquefasciatus (Insecta: diptera: culicidae). Parasitol Res 2013; 112: 1053–1063.

72.

Khooshe-Bast

Sahebzadeh

Ghaffari-Moghaddam

, et al. Insecticidal effects of zinc oxide nanoparticles and Beauveria bassiana TS11 on Trialeurodes vaporariorum (westwood, 1856)(Hemiptera: aleyrodidae). Acta Agric Slov 2016; 107: 299–309.

73.

Ghramh

Al-Ghamdi

Mahyoub

, et al. Chrysanthemum extract and extract prepared silver nanoparticles as biocides to control Aedes aegypti (L.), the vector of dengue fever. J Asia-Pac Entomol 2018; 21: 205–210.

74.

Devi

Murugan

Selvam

. Green synthesis of silver nanoparticles using Euphorbia hirta (Euphorbiaceae) leaf extract against crop pest of cotton bollworm, Helicoverpa armigera (Lepidoptera: noctuidae). J Biopestic 2014; 7: 54.