OCL 2025, 32, 4DOI: 10.1051/ocl/2024035© M.A. Qayyoum et al., Published by EDP Sciences, 2025

This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Research Article

Fatty acids from soybeans: compatibility with Panonychus citri (Acari: Tetranychidae) and its two predators☆

Acides gras de soja : Compatibilité avec Panonychus citri (Acari : Tetranychidae) et ses deux prédateurs

Muhammad Asif Qayyoum¹,2* orcid, Bilal Saeed Khan³, Zi-Wei Song², Tian-Ci Yi¹, Rehan Inayat¹ orcid, Muhammad Irfan Akram⁴ orcid, Syed Husne Mobarak¹ and Dun-Song Li²*

¹ Institute of Entomology, Guizhou University, Guiyang Guizhou, 550025, PR China
² Key Laboratory of Green Prevention and Control on Fruits and Vegetables in South China Ministry of Agriculture and Rural Affairs/Guangdong Provincial Key Laboratory of High Technology for Plant Protection/Plant Protection Research Institute, Guangdong Academy of Agriculture Sciences, 7 Jinying Road, Tianhe District, Guangzhou, 510640, PR China
³ Department of Entomology, Faculty of Agriculture, University of Agriculture, Faisalabad, Punjab, Pakistan
⁴ Department of Entomology, Faculty of Agriculture and Environment, The Islamia University of Bahawalpur, Bahawalpur 63100, Punjab, Pakistan

* Corresponding: asifqayyoum@gmail.com; dsli@gdppri.cn

Received: 11 July 2024 Accepted: 17 December 2024 Published online: 24 January 2025

Abstract

Soybean oil is a significant alternative to synthetic chemicals for environmentally friendly and sustainable pest control. This study evaluated soybean oil and its fatty acids (palmitic, oleic, and stearic acids; individually) for their acaricidal and repellent effects against Panonychus citri (Tetranychidae) and its predators [Neoseiulus californicus and Neoseiulus barkeri [Phytoseiidae]) using laboratory foliar dipping and topical spray methods. The LC₅₀ (Lethal Concentration) values for palmitic, oleic, stearic acids, and soybean oil against P. citri were 0.86%, 0.95%, 0.56%, and 0.05% for LDM (Leaf-dipping Method) and 11.92%, 5.34%, 1.46%, and 0.07% for TSM (Topical Spray Method). Soybean oil has maximum attraction (46.67 ± 3.6%) and significantly higher acaricidal effectiveness (46.25 ± 0.98%) compared to acids except oleic acid (50.83 ± 1.22%) against P. citri. Soybean oil showed the least toxicity, with the highest LT₅₀ (Lethal Time) values for N. californicus (LDM: 1.19 h, TSM: 1.27 h). While soybean oil caused a less significant reduction in fertility and lower lethal efficacy (0.83 ± 0.83%) on predatory mites compared to P. citri. Compared to soybean oil, oleic acid reduces fertility rate (27 ± 1.60%) and is an effective repellent (65-75%) against N. californicus and N. barkeri and reduces prey consumption (15-16%) and laying eggs (0.75 ± 0.47) on treated surfaces compared to other treatments. Palmitic acid increases prey consumption (27.5 ± 3.28%) and fertility rates (5.00 ± 0.71) of N. californicus. Palmitic acid, despite being less toxic to P. citri, effectively repels predators, while soybean oil and oleic acid have stronger repellent effects. Leaf dipping was less effective than topical spray. Soybean oil, with its lower mortality rates and sublethal effects on reproduction and behavior, is a strong candidate for integrated pest management strategies. Oleic and palmitic acids, though effective, have repellency to beneficial predators.

Résumé

L’huile de soja est une alternative importante aux produits chimiques synthétiques pour une lutte antiparasitaire durable et respectueuse de l’environnement. Cette étude a évalué l’huile de soja et ses acides gras (acides palmitique, oléique et stéarique ; individuellement) pour leurs effets acaricides et répulsifs contre Panonychus citri (Tetranychidae) et ses prédateurs (Neoseiulus californicus et Neoseiulus barkeri (Phytoseiidae)) en utilisant des méthodes de trempage foliaire et de pulvérisation topique en laboratoire. Les valeurs de la LC50 (concentration létale) pour les acides palmitique, oléique, stéarique et l’huile de soja contre P. citri étaient de 0,86 %, 0,95 %, 0,56 % et 0,05 % pour la méthode de trempage foliaire (LDM) et de 11,92 %, 5,34 %, 1,46 % et 0,07 % pour la méthode de pulvérisation topique (TSM). L’huile de soja présente une attraction maximale (46,67 ± 3,6 %) et une efficacité acaricide significativement plus élevée contre P. citri (46,25 ± 0,98 %) par rapport aux acides gras, à l’exception de l’acide oléique (50,83 ± 1,22 %),. L’huile de soja a montré la toxicité la plus faible, avec les valeurs de temps létal (LT50) les plus élevées pour N. californicus (LDM : 1,19 h, TSM : 1,27 h). L’huile de soja a entraîné une réduction moins importante de la fertilité et une efficacité létale plus faible (0,83 ± 0,83 %) sur les acariens prédateurs par rapport à P. citri. Comparé à l’huile de soja, l’acide oléique réduit le taux de fertilité (27 ± 1,60 %) et est un répulsif efficace (65-75 %) contre N. californicus et N. barkeri, réduit la consommation de proies (15-16 %) et la ponte (0,75 ± 0,47) sur les surfaces traitées par rapport aux autres modalités. L’acide palmitique augmente la consommation de proies (27,5 ± 3,28 %) et les taux de fertilité (5,00 ± 0,71) de N. californicus. L’acide palmitique, bien que moins toxique pour P. citri, repousse efficacement les prédateurs, tandis que l’huile de soja et l’acide oléique ont des effets répulsifs plus importants. La technique de trempage des feuilles a été moins efficace que la pulvérisation topique. L’huile de soja, avec ses taux de mortalité et ses effets sublétaux plus faibles sur la reproduction et le comportement, est un candidat pertinent pour les stratégies de lutte intégrée contre les ravageurs. Les acides oléiques et palmitiques, bien qu’efficaces, ont un effet répulsif sur les ennemis naturels prédateurs.

Key words: citrus red mite / predatory mites / soybean oil / acaricidal efficacy / repellency

Mots clés : acarien rouge des agrumes / acariens prédateurs / huile de soja / efficacité acaricide / effet répulsif

☆

Contribution to the Topical Issue: “Non-Food Uses Of Oil- And Protein- Crops / Usages Non Alimentaires des Oléoprotéagineux”.

Highlights

Soybean oil, with its low mortality rates and sublethal effects on reproduction and behavior, is a promising candidate for integrated pest management strategies.

Oleic acid was found toxic against Panonychus citri and repellent against predatory mites.

Palmitic acid attracts all mites, increasing prey consumption and fertility rates of Neoseiulus californicus (McGregor).

N. barkeri (Hughes) exhibited a favorable response to stearic acid, demonstrating higher prey consumption and fertility rate.

1 Introduction

Food waste is a crucial global issue that affects the environment, economy, and society. Wastage of food: Almost one-third of all food produced (approx. 1.3 billion tons/year) for human consumption is lost or wasted annually (Derqui et al., 2016; Falasconi et al., 2019). Food waste is a major global environmental and economic challenge; according to the Food and Agriculture Organization (FAO), there are several reasons for food waste, including production, processing, retailing, and consumption leading to a lack of public awareness resulting in Greenhouse Gas (GHG) emissions and Resource Depletion likewise (Zuin and Ramin, 2018; Forster-Carneiro et al., 2013; Perlatti et al., 2014; Visakh et al., 2023; Panzella et al., 2020) etc. Several sustainable strategies like composting and bioenergy production from food waste have been suggested to overcome these challenges (Kwanyun et al., 2023; Paritosh et al., 2017).

Kitchen waste can be used as a natural pesticide, reducing human health risks and environmental pollution (Iqbal et al., 2022). This practice aligns with sustainable farming systems, as it reduces chemical pesticides and offsets excess food waste. It also aligns with integrated pest management principles, promoting sustainability in agriculture by integrating biopesticides derived from kitchen waste into consistent pest control strategies (Conrad et al., 2018; Stenberg, 2017). In China’s restaurant industry, kitchen waste generates significant waste, with 80% used on pig farms. Soybean oil (Glycine max), a valuable raw material for food, feed, chemical, and healthcare industries, is consumed annually at 17.8 million tons (Patton, 2023). Burning cooking oil poses environmental and health risks, while soybean oil’s long-chain fatty acids can be used as an environmentally friendly insecticidal substitute with attractive and repellent properties (Qayyoum et al., 2021a; 2021b). Soybean oil bodies are capsules 250–700 µm diameter containing neutral lipid droplets, natural emulsifiers, alkaline proteins, and micronutrients (Zaaboul et al., 2022). It is rich in saturated, monounsaturated, and polyunsaturated fats (alpha-linolenic, linoleic, stearic, palmitic, and oleic acids) (Saraiva et al., 2020). Linoleic acid, a vital component of vegetable oil, led to attractive reactions (Buehlmann et al., 2014). According to various studies, alpha-linolenic acid and linoleic acid found in southern cattails can alter the permeability of plant plasma membranes and destroy chloroplast membranes (Wu et al., 2006). In previous studies, vegetable oil’s short-chain compound (palmitic acid) gave equal repellency to synthetic chemicals (Mullens et al., 2009). Oleic, stearic, and palmitic acids had significant toxic effects on Callosobruchus maculatus (Coleoptera: Bruchidae) and reduced longevity, fecundity, and hatchability of eggs (Aider et al., 2016).

Panonychus citri, a citrus red mite, is a significant pest in citrus orchards worldwide. Current control measures include pesticide spraying, which can cause toxic effects (Karmakar, 2019). IPM strategies have been used in China since the 1970s (Liu et al., 2019), but most studies focus on control effectiveness, pesticide resistance, and management (Xiao et al., 2010). The focus of IPM programs should be on minimizing toxicity to natural beneficial fauna rather than causing significant harm to the target species (Tsolakis and Ragusa, 2008). Natural and naturally available predators primarily control insect pest populations, but phytoseiidae have been used as biological control agents for various phytophagous mites (Chang and Kareiva, 1999). Among the phytoseiids, Neoseiulus californicus and N. barkeri are commonly used as augmented biological control against various mites and insect pests (Mendel and Schausberger, 2011; Qayyoum et al., 2021c). N. californicus and N. barkeri, commercially available since the 1980s, effectively control spider mites in crops like strawberries and tomatoes, reducing reliance on chemical pesticides (Fang et al., 2013; Silva, 2023). N. californicus is a versatile predator known for its adaptability and ability to thrive in various environments. It can consume spider mites like Tetranychus urticae and P. citri, effectively suppressing populations of P. citri (Katayama et al., 2006; Ebrahim et al., 2014). N. californicus can maintain its population even with low prey densities (Abad-Moyano et al., 2010; Greco et al., 2005), feeding on pollen. On the other hand, N. barkeri, a generalist predator, exhibits different predation dynamics, particularly in intraguild interactions (Momen and Abdel-Khalek, 2021; Haghani et al., 2015) (Abad-Moyano et al., 2010; Çakmak et al., 2006). Both species coexist and contribute to pest suppression in agricultural settings (Ahn et al., 2010; Hoddle et al., 2000).

Soybean oil can easily penetrate eggs, and the soft integument of T. urticae inhibits the rotational movement of the embryonic liquid (Oliveira et al., 2017; Takeda et al., 2020). It can be used in combination with predatory mites (N. baraki and Typhlodromus ornatus) (Oliveira et al., 2020; Saraiva et al., 2020; Teodoro et al., 2020). Higher rates resulted in greater phytotoxicity (Baker et al., 2018), but vegetable oils have a broad-spectrum effect against soft-bodied insect pests (Alexenizer and Dorn, 2007). However, their selection should be strictly evaluated against natural enemies and targeted pests (Guedes et al., 2016; Tsolakis and Ragusa, 2008). Few studies have been conducted on evaluating fatty acids against P. citri and its predators, except for previous research. We tested three fatty acids (stearic acid, palmitic acid, and oleic acid) (synthetically available in the market) along with soybean oil for their toxicity and repellency (behavioral responses) effects against P. citri, N. californicus, and N. barkeri. The findings will provide insights into the potential use of these compounds for integrated pest management strategies.

2 Materials and methods

2.1 Mites culture

P. citri were reared under controlled laboratory conditions according to Qayyoum et al. (2021a, 2021b). N. californicus was collected from Carica papaya (Caricaceae) in Guangzhou, China (N 23.15, W 113.33) in 2011, as detailed in Qayyoum et al. (2021c). N. californicus was maintained using mixed stages of T. urticae on bean [Phaseolus vulgaris (Fabaceae]) leaves placed on water-saturated sponges (10 cm in diameter, 3 cm thick) in plastic boxes (15 cm × 15 cm × 6.5 cm). N. barkeri was reared on Tyrophagus putrescentiae (Acaridae), which was collected from wheat bran, and colonies were set up in Petri dishes (9 cm in diameter) with dry yeast; the Petri dishes were placed on water-saturated sponges (13 cm in diameter, 3 cm thick) in plastic circular boxes (20 cm in diameter) with water. All cultures were kept in climatic incubators (25 ± 1 °C, 65 ± 10% RH, and 16:8 h L:D) (Zheng et al., 2017). All predatory mites were reared for over three generations on P. citri for prey-predator synchronization.

2.2 Chemicals

The Institute of Zoology, Guangdong Academy of Sciences, Guangzhou, China, provided soybean oil (G. max) as a trial product (Kitchen waste soybean oil) against the citrus red mite. Soybean oil contains 54% of Linoleic acid ethyl ester (C₂₀H₃₆O₂), 8% of Hexadecanoic acid, ethyl ester (palmitic acid = CH₃ (CH₂)₁₄COOH), 5% 9-Octadecenoic acid (Z)-, methyl ester (Oleic acid = C₁₉H₃₆O₂) and 1.8% of Octadecanoic acid, ethyl ester (Stearic acid = C₁₈H₃₆O₂).

Fatty acids were purchased from local markets: palmitic, 99% granular, purchased from Tianjin Fuchen chemicals reagents factory; stearic acid, 99% granular, purchased from Fuchen reagents factory and Oleic acid liquid purchased from Tian Fuyu Fine Chemicals Co. Ltd. Note: We have not used the linoleic acid because in small amounts it has maximum toxicity to predators and causes phytotoxicity in plantations.

Note: Linoleic acid is a significant part of soybean oil, but we did not select it because it is difficult to mix with water.

2.3 Chemical preparation

Two percent (0.50 mg) of acids were added to the distilled water with 1% tween and 18% ethanol. The homogenous mixture solution was made by heating it and stirring it for 2–5 min on the low-flamed burner. After attaining a solution, we used five different concentrations (2%, 1%, 0.5%, 0.25%, and 0.124%) for each fatty acid for soybean oil, followed (Qayyoum et al., 2021a, 2021b) with four concentrations (0.12, 0.06%, 0.03%, and 0.013%).

All concentrations were mixed into the tap water for further use, with mortality ranging from 10% to >90%. The data was collected at 24 h, 48 h, 72 h, and 96 h intervals to obtain said mortality percentage. We also used 1% tween and 18% ethanol in water as control treatments in all experiments.

The lethal concentrations obtained through the leaf dip methods were further used for lethality effect and behavioral responses.

2.4 Experimental methodology

The toxicities of all chemicals were calculated using the modified leaf dip method (He et al., 2011) and topical spray method (see supplement data). Green and healthy leaves were collected from the untreated lemon field and stored in the refrigerator for 24 hours. Before cutting leaf discs, each leaf was washed with water thoroughly and dried using a paper towel. Each leaf disc (≈3 cm²) was fully dipped for 5 seconds and shifted on the water-saturated sponge in the plastic container. It was surrounded by wet tissue paper to avoid mites’ escape. Thirty adult female mites (same age as laboratory-reared strain − ≥1-3 days old adults) were released on each leaf after 10–15 min of drying the leaf, with three replications. Water-dipped leaves were used as the control treatment. A bioassay test was performed by maintaining the 26 ± 1 °C, 16:8h (L:D) photoperiod, and 75% relative humidity in an incubator (Qayyoum et al., 2021).

Each chemical’s selected concentrations were also sprayed with a fine mist sprayer pump (perfume spray nozzle). A total of 4–6 times the chosen concentrations were sprayed on the leaf discs. The data of dead mites and the number of eggs were counted with specific time intervals using both methods.

For lethality effectiveness, we used lethal doses obtained by leaf dipping. The topical spray method provided high concentrations of all fatty acids (more than 1%) that can have a phytotoxic effect on plantations. The lethality of each LC₅₀ was checked against both predators and prey (P. citri), and data were recorded at 4 h, 8 h, 12 h, 24 h, 48 h, 72 h, and 96 h intervals. We also inspected the impact of lethality on the total number of eggs, eggs hatching %, and % offspring reached the adult stages (Adultery %). We used 40 eggs to check the hatching % and % adultery of offspring.

We also used the leaf dip method for behavioral experiments, a lethal dose of each chemical against P. citri. The behavioral responses of N. californicus and N. barkeri were evaluated on the repellency of treated leaf discs, and prey consumption was recorded. Two plastic strips (1 cm in diameter) were used to make an “X-shaped” cross-bridge between four equally spaced circular cells. Ten female adults of ≥1–3 days old (He et al., 2011) were released in each cell. Ten N. californicus and N. barkeri were individually released on the cross point for different experimentations. The above methodology was performed to compare the chemical with the control treatment in a choice test using two experimental methods by replicating four times. The number of predatory mites present and the number of prey consumed were recorded after 24 hours of predatory mites’ release.

The behavioral response of choice test was used as described by Roh et al., (2013). We used more than 7 months of citrus plantation with almost 1–2 feet in height, which bears the insect and phytotoxic effect. We clipped all leaves except two leaves from different sides. One leaf was dipped with solution (LC₅₀) of each solution for 10 seconds, and the second leaf was left blank. After air-drying, 30 mites of female P. citri adults were released on the stem. The adult mite mortality and the total number of eggs on the treated and untreated were recorded after 24-hour mite inoculation. This section of the experiment was replicated four times.

2.5 Statistical analysis

The five selected concentrations of each acid (2%, 1%, 0.5%, 0.25%, and 0.124%) were used to calculate the lethal concentrations (LC₅₀) along with lethal time (LT₅₀). The confidence interval of 95% was also estimated with a log-probit regression model using SPSS version 22.0 (IBM-Corp., 2013). The data between the two treatments (treated vs. untreated (Choice test)) was compared using an independent samples t-test, suggesting that both treatments were unequal for behavioral response experiments.

ANOVA was analyzed using treatment and time as fixed factors (lethal efficacy of soybean and fatty acids against Panonychus citri and its predators to check mortality, number of eggs, hatching percentage, and eggs reached adultery). In contrast, the number of mites was a dependent variable. If the interaction was significantly observed, the data was sliced by time. All analysis was done using SPSS version 22.0 (IBM-Corp., 2013).

3 Results

3.1 Toxicity against Panonychus citri and its predators

The toxic effect of different concentrations of each acid resulted in lethal and sublethal effects, as shown in Table 1. The LC₅₀ of palmitic, oleic, stearic acids, and soybean oil were valued at 0.86%, 0.95%, 0.56%, and 0.05%, respectively, for the leaf dipped method (LDM) and 11.92%, 5.34%, 1.46%, and 0.07%, respectively for the topical spray method against P. citri (Tab. 1). The leaf dipping method resulted in quick mortality compared to the topical spray method (TSM) with lower lethal time (LT₅₀) except for soybean oil (1.19) and palmitic acid (1.27) against Neoseiulus californicus. Soybean oil resulted lower LT₅₀ comparison value (0.29) for LDM (Slope ± SE = 1.49 ± 2.21, χ² (df = 2) = 0.02, P = 0.98) compared to TSM (Slope ± SE = 0.80 ± 1.24, χ² (df = 2) = 0.01, P = 0.99) which mean TSM resulted lowest effectiveness against N. barkeri (Fig. 1).

The ratio between LDM and TSM was higher (1.27) for palmitic acid, as LDM responded slower than TSM. Soybean oil had significantly different effects across methods and mites used, while oleic acid had a more significant impact. Stearic acid (20.26 h, Slope ± SE = 2.37 ± 0.58, χ² (df = 2) = 2.12, P = 0.35) and palmitic acid (111.06 h, Slope ± SE = 3.51 ± 1.38, χ² (df = 2) = 0.29, P = 0.86) resulted maximum impacted against P. citri and N. barkeri respectively. Soybean oil was less effective against predatory mites than fatty acids used, as shown in figure 1 (see Tab. S1).

We also checked the lethal effect against P. citri and its predators (N. californicus and N. barkeri) with a time interval of 4, 8, 12, 24, 48, 72, and 96 h after exposure (Tab. S2, Fig. 2, Fig. S4). The lethal time (LT₅₀) of oleic acid was shortest (Slope ± SE = 2.33 ± 0.26, χ² (df = 5) = 8.22, P = 0.15) during leaf dip method with 0.79 compared value between LDM (20.73 h) and TSM (26.36 h), followed by soybean oil (1.09), stearic acid (1.074), and palmitic acid (1.33) against P. citri. The lethality activity of oleic acid was more toxic against N. californicus and N. barkeri, with TSM yielding 20% and 50% lower efficacy than LDM.

In contrast, stearic acid resulted in more effectiveness using LDM, which resulted in more than 6 times less (6.21) efficacy against N. barkeri. Oleic acid seems more effective against P. citri with a shorter lethal time, but its effectiveness against both is unsuitable for our recommendations against both predators. Palmitic acid has the lowest effectiveness compared to other treatments with values above 1 (although LDM was a better choice than TSM). Control treatment performs a similar pattern as soybean oil but with a higher lethal time than other treatments except against N. californicus compared to stearic acid and palmitic acid (Tab. S2, Fig. 2).

The lethal impact of acids (fatty acids) and soybean oil was tested against P. citri, N. californicus, and N. barkeri, with mortality (%) after 24 hours and a total number of eggs laid by females. Lethality resulted significantly differently within treatments for prey and predators except for the mortality of N. californicus during the topical spray method (Tab. 2). All the treatments used gave significant mortality % after 24 hours against P. citri compared to the control treatment. Oleic acid showed 50% mortality using the leaf-dipped method, which decreased to 29.5% using the tropical spray method. Soybean oil efficiency was like oleic acid but slightly decreased mortality from 46.25% to 43.75% (LDM to TSM). The mortality trend after 24 hours for LDM was Oleic acid = soybean oil > stearic acid > palmitic acid > control. In contrast, TSM, soybean oil > palmitic acid > stearic acid > oleic acid > control (Tab. 2). The impact of the lethality of treatments used on the next generations was checked by examining the egg-hatching percentage and reached adultery. Soybean oil had a more substantial impact on the eggs of infected females hatching (75%), and hatched individuals reached adultery (77.6%). All acids perform similarly to each other with significantly different control treatments. Compared to LDM, the TSM section gave slightly different results, as soybean oil significantly impacted the hatching percentage. Still, the adultery percentage was more impacted by palmitic acid (Tab. S3).

Higher mortality (%) in adult females resulted in fewer eggs being laid. Higher mortality (%) resulted in more eggs for P. citri, N. californicus, and N. barkeri during the topical spray method. Still, it lowered than controlled treatments (Tab. 2). Palmitic acid also showed slightly higher (1%) phytotoxicity than other treatments. Soybean oil similarly impacted the egg hatching percentage out of 40 eggs against predatory and citrus red mites. In contrast, the rate of adultery was more affected by the leaf dip method (Fig. 3, Tab. S3). Palmitic acid maximum impacted P. citri using LDM while less effective against N. barkeri while palmitic impacted less by using LDM compared to TSM. The lowest hatching percentage was observed against N. barkeri during LDM, while the maximum was observed against P. citri during TSM. In contrast, the rate of adultery was observed to be almost similar in the methods used and prey and predators. All treatments impacted predators significantly and P. citri compared to the control treatment (Fig. 3, Tab. S3).

Table 1

Toxicity of fatty acids of soybean plant against Panonychus citri in two application methods. All units are used in percentage V/V.

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Fig. 1

Lethal time (LT₅₀) ratio between the leaf dip method and topical spray method of exposure to soybean oil and fatty acids at different concentrations of each treatment over observational time (24 h, 48h, 72h, and 96h) against Panonychus citri and its predators.

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Fig. 2

Lethal time (LT₅₀) ratio between the leaf dip method and topical spray method of exposure to soybean oil and fatty acids at a lethal concentration of each treatment over observational time (4 h, 8 h, 12 h, 24 h, 48 h, 72 h, and 96 h) against Panonychus citri and its predators.

Table 2

The lethal efficacy of soybean and fatty acids against Panonychus citri and its predators was exposed using leaf dip and topical spray after 24 h of exposure.

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Fig. 3

The lethal efficacy of soybean and fatty acids impact egg hatching percentage and the percentage of hatched eggs reached adultery when exposed to the parental population of Panonychus citri and its predators using leaf dip and topical spray methods.

3.2 Behavioral responses

The behavioral responses were checked by the movement of mites towards (attractiveness) and away (repel) from treated surfaces. The attractiveness and repellency of palmitic (t-value: −5.83, p-value: 0.01) and stearic (t-value: −2.67, p-value: 0.04) acids significantly affected the movement of P. citri. Both acids attracted 41 to 42% of adults towards them. In comparison, they repelled 58.33% (Tab. 3). This attraction was increased from 40 to 45% to attract predatory mites compared to other treatments (Tab. 4). The repellent effect of soybean oil and oleic acid was significantly higher (For N. californicus: (Soybean oil: t-value: −5.28, p-value: 0.002, Oleic acid: t-value: −4.66, p-value: 0.003), and for N. barkeri (Soybean oil: t-value: −3.57, p-value: 0.012; Oleic acid: t-value: −5.82, p-value: 0.01)) than palmitic and stearic acids. The study found that P. citri showed a more significant, non-significant attraction to treated surfaces than palmitic and stearic acids (Tabs. 3 and 4).

The total number of eggs laid by adult females of P. citri was significantly lower on leaves dipped with oleic acid, followed by palmitic acid, soybean oil, and stearic acid (Tab. 3). Oleic acid also considerably affected the total number of egg production by both adult females of N. californicus and N. barkeri with trends of oleic acid > soybean oil > stearic acid > palmitic acid and oleic acid > soybean oil > palmitic acid > stearic acid, respectively (Tab. 4).

The lethal effect of soybean oil and oleic acid (leaves dipped) has a significant impact on the movement of N. californicus (by repelling 65% more mites away from treated surfaces), with the lowest prey (P. citri) consumption rate (%) on the treated surfaces. Due to non-significant movement between treated and untreated surfaces of palmitic and stearic acids, N. californicus consumes more P. citri. The movement of N. barkeri on treated leaves with palmitic acid and untreated leaves was not significant compared to the other treatment results. In contrast to N. californicus, N. barkeri led to significantly lowest prey consumption after 24 h on palmitic-treated surfaces, even though the movement was non-significantly different between treated and untreated surfaces (Tab. 4).

Table 3

The numbers of female Panonychus citri attracted to, and the numbers of eggs oviposit on the citrus leaves treated (LC50) or untreated with soybean oil and its fatty acids in choice tests.

Table 4

The numbers of female Neoseiulus californicus (McGregor) and Neoseiulus barkeri Hughes attracted to, and the numbers of eggs oviposition on the citrus leaves treated (LC50) or untreated with soybean oil and its fatty acids in choice tests.

4 Discussion

In the search for novel plant-based compounds for IPM programs of different pests, we selected long-chained saturated and unsaturated fatty acids from soybean oil. This work demonstrated that soybean oil and fatty acids (palmitic acid, oleic acid, and stearic acid) exhibited acaricidal activity as well as reducing the total number of eggs of P. citri and its predators (N. californicus and N. barkeri). In our previous work, we documented that soybean oil acts as an alternative to synthetic chemicals by impacting the dispersal and behavioral response of P. citri (Qayyoum et al., 2021a, 2021b). Although a few articles have been published related to the impact of fatty acids on acaricidal or insecticidal activity (Li, 2016; Mohamad et al., 2013; Sims et al., 2014; Twining et al., 2018; Zhu et al., 2018). The first time, we demonstrated the impact of three fatty acids against P. citri and its two common predators.

In the acaricidal lethal efficacy test, oleic acid impacted maximum on the P. citri with the lowest LT₅₀, while palmitic acid was found to be less toxic against all tested mites. Oleic acid gave 25% mortality against Callosobruchus maculatus instead of 50% against P. citri (Tab. 3). The fecundity rate of P. citri was also significantly reduced compared to findings with higher toxic effects. It stated that the toxicity of fatty acid increased with the increase of carbon atoms in its molecular weight (Sims et al., 2014) as oleic acids (C₁₉H₃₆O₂) have a higher number of carbon atoms than palmitic acid (C₁₈H₃₆O₂). Still, this statement failed when compared with the molecular formula of stearic acid (C₂₀H₄₀O₂). Sims et al. (2014) also showed that more toxicity was observed in a compound with an odd number of carbon atoms, as in oleic acid in a recent study.

We also found that the topical spray method needs more time to kill 50% of the offered pest population than the leaf-dipped method, which differs from (Sims et al., 2014) results (similar toxicity in both application methods). The variation of results from previous studies depends on the nature of the chemical and pest species. Soybean oil toxicity was significantly higher after oleic acid against P. citri due to a mixture of many fatty acids, as observed by Hatem et al. (2009). Due to the presence of Linoleic acid and other along-chain unsaturated fatty acids in soybean oil (Oliveira et al., 2017), soybean oil acts as toxic and has a repellent effect on arthropods (Hieu et al., 2015). A similar effect was observed against Typhlodromus ornatus (Acari: Phytoseiidae) (Saraiva et al., 2020) and Stomoxys calcitrans (Diptera, Muscidae) (Hieu et al., 2015) after 24 hours of exposure.

Maximum toxicity with lower egg production is a common phenomenon in the case of P. citri. Still, oleic acid revealed no toxicity or less toxicity against both predatory mites, which also induces the production of their eggs compared to other stearic acid or controlled treatments. However, the number of eggs remains almost similar in both application methods. We concluded that with maximum time availed with a maximum number of mites, the production of eggs also increased (Sabelis, 1985).

Most fatty acids are part of plant cuticles, which play an essential role by interfering with plant and phytophagous insects. Applying fatty acids alone or a combination of different fatty acids changes the behavior of different insects and mites (Qayyoum et al., 2021a, 2021b). The role of attraction or deterring any arthropod depends on its structure and length: long-chain unsaturated fatty acids inhibited the settlement of Myzus persicae (Hemiptera: Aphididae), but long-chain saturated fatty acids showed an attractive effect (Santana et al., 2012).

Due to the above qualities, we try to confirm the repellency and attractiveness of fatty acids and soybean oil against P. citri, N. californicus, and N. barkeri. We resulted in significant mites repelled from treated surfaces (58.33%) except for soybean oil (Qayyoum et al., 2021a, 2021b) and oleic acid against P. citri. This non-significant repellency and attractiveness were also confirmed against T. urticae by using Myrtaceae essential oils (Roh et al., 2013) and against M. persicae by using Medium-Chain Fatty Acids from Eugenia winzerlingii (Myrtaceae) (Cruz-Estrada et al., 2019). In contrast, soybean oil resulted in more significant repellency against Neoseiulus baraki after one hour of exposure (Oliveira et al., 2017) and T. ornatus (Saraiva et al., 2020). Like the results of N. baraki (Oliveira et al., 2017) and T. ornatus against predatory mites, soybean oil and oleic acid forced the majority of N. californicus and N. baraki away from treated surfaces (Tab. 4).

This response against different insects due to their anti-feeding and reduction in oviposition depends on species-specific chemoreceptors like sensilla in insect antennae (Seenivasagan et al., 2013). This repellent behavior also reduced the number of eggs on the treated surfaces (Tab. 4) as the impact of Datura stramonium against T. urticae (Kumral et al., 2010) as fatty acids penetrate the integument of mites like T. urticae, which inhibits the rotational movement of embryonic liquid by resulting in quick toxicity and less egg production (Takeda et al., 2020; Tsolakis and Ragusa, 2008).

The attractive behavior of predatory mites is due to the presence of detoxifying enzymes (monooxygenases (Roush and Plapp Jr, 1982), esterases (Anber and Oppenoorth, 1989), and glutathione-S-transferases (Fournier et al., 1987)). Attraction toward prey is a social olfactory interaction cue, which is a predator-borne chemosensory cue for the HIPVs (herbivore-induced plant volatiles) recognition (Hettyey et al., 2015; Sabelis and Dicke, 1985; Saraiva et al., 2020; Schausberger et al., 2020). As a long-chain saturated fatty acid, palmitic acid has an attractive effect (Castillo et al., 2010; Santana et al., 2012). In contrast, we find neither significant attractiveness nor repellency of predatory mites towards treated (palmitic acid) and untreated surfaces with an equal number of prey (Tab. 4). However, this phenomenon significantly impacted the prey consumption and fecundity rates, which need more detailed explanations (Cisak et al., 2012).

5 Conclusion

This study provides valuable insights into the toxic effects of three fatty acids—palmitic, oleic, and stearic acids—on Panonychus citri (the citrus red mite) and its predatory mites (Neoseiulus californicus and Neoseiulus barkeri). Each fatty acid exhibited distinct lethal and sublethal effects, with oleic acid demonstrating the most effective toxicity against P. citri, followed by stearic and palmitic acids. Notably, soybean oil, which contains a unique combination of these fatty acids, had a more pronounced impact on P. citri compared to the individual acids, suggesting that the composition of fatty acids in soybean oil may enhance its overall toxicity. However, its effect on the predatory mites was less favorable, with soybean oil showing lower efficacy than the individual fatty acids in terms of both lethal impact and predator mortality.

Considering the balance between pest control and predator preservation, oleic acid emerged as a potentially more effective agent for targeting P. citri due to its shorter lethal time, though it had a more significant repellent effect on the predators, making it less ideal for integrated pest management. On the other hand, palmitic acid, while less effective against P. citri, demonstrated a more balanced impact on both pests and predators. Stearic acid also exhibited notable efficacy but was more variable in its effects depending on the application method.

In terms of alternative treatments, this study highlights the potential for using soybean oil, but a combination of two or more fatty acids could offer a more tailored solution, balancing toxicity against P. citri while minimizing the impact on beneficial predatory mites. Further research is needed to explore the use of other oils with different fatty acid compositions that may be more suited for this purpose. Oils rich in specific fatty acids may offer better control over pest populations while preserving beneficial species, ensuring the sustainability of pest management strategies. Thus, while soybean oil shows promise as an effective pest control agent, a more nuanced approach, potentially incorporating specific fatty acids or blends, may provide optimal results for both controlling P. citri and protecting predatory mites.

Acknowledgments

All authors acknowledged the support of the Guangdong provincial government, China, and the Guangdong Academy of Agricultural Sciences for their support and facilities. We also acknowledged the supportive efforts of Prof. Zhang Bao-Xin and Yuan Zheng (Bio-control Lab. Assistant, PPRI, GAAS, China) and anonymous reviewers. China Litchi and Longan Research System Foundation (CARS-32- 12), National Key R&D Program of China (2017YFD0202000), China Postdoctoral Research Foundation (229807 & 348577), Dean Fund of Guangdong Academy of Agricultural Sciences (BZ201906), and Discipline team-building projects of Guangdong Academy of Agricultural Sciences (13th five-year period) were the support funding agencies of this research work.

Conflicts of interest

The authors declare they have no competing interests.

Supplementary Material

Figure S1. Toxicity of all treatments against Panonychus citri.

Figure S2. Toxicity of all treatments against Neosiulus californicus.

Figure S3. Toxicity of all treatments against Neosiulus barkeri.

Figure S4. Lethality of treatments against Panonychus citri, Neoseiulus californicus, and N. barkeri.

Table S1. Lethal time (LT₅₀) of Panonychus citri and its predators exposed to soybean oil and fatty acids by using leaf dip method and topical spray method.

Table S2. Lethal time (LT₅₀) of Panonychus citri and its predators exposed to LC₅₀ soybean oil and fatty acids using leaf dip and topical spray methods.

Table S3. Lethal efficacy of soybean and fatty acids impact egg hatching percentage and percent hatched eggs reached to the adultery when exposed to the parental population of Panonychus citri and its predators exposed by leaf dip method and topical spray method.

(Refer to website)

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Cite this article as: Qayyoum MA, Khan BS, Song Z-W, Yi T-C, Inayat R, Akram MI, Mobarak SH, Li D-S. 2025. Fatty acids from soybeans: compatibility with Panonychus citri (Acari: Tetranychidae) and its two predators. OCL 32: 4. https://doi.org/10.1051/ocl/2024035.

All Tables

Table 1

Toxicity of fatty acids of soybean plant against Panonychus citri in two application methods. All units are used in percentage V/V.

In the text

Table 2

The lethal efficacy of soybean and fatty acids against Panonychus citri and its predators was exposed using leaf dip and topical spray after 24 h of exposure.

In the text

Table 3

The numbers of female Panonychus citri attracted to, and the numbers of eggs oviposit on the citrus leaves treated (LC50) or untreated with soybean oil and its fatty acids in choice tests.

In the text

Table 4

The numbers of female Neoseiulus californicus (McGregor) and Neoseiulus barkeri Hughes attracted to, and the numbers of eggs oviposition on the citrus leaves treated (LC50) or untreated with soybean oil and its fatty acids in choice tests.

In the text

All Figures

thumbnail
Fig. 1

Lethal time (LT₅₀) ratio between the leaf dip method and topical spray method of exposure to soybean oil and fatty acids at different concentrations of each treatment over observational time (24 h, 48h, 72h, and 96h) against Panonychus citri and its predators.

In the text

thumbnail
Fig. 2

Lethal time (LT₅₀) ratio between the leaf dip method and topical spray method of exposure to soybean oil and fatty acids at a lethal concentration of each treatment over observational time (4 h, 8 h, 12 h, 24 h, 48 h, 72 h, and 96 h) against Panonychus citri and its predators.

In the text

thumbnail
Fig. 3

The lethal efficacy of soybean and fatty acids impact egg hatching percentage and the percentage of hatched eggs reached adultery when exposed to the parental population of Panonychus citri and its predators using leaf dip and topical spray methods.

In the text

Table 1

Toxicity of fatty acids of soybean plant against Panonychus citri in two application methods. All units are used in percentage V/V.

Treatments
Leaf dip method

LC₃₀ (95% CI)
LC₅₀ (95% CI)
LC₉₀ (95% CI)
Slope ± SE
Z
ᵪ² (df=3)
P1
P2

Palmitic acid
0.137 (0.003-0.309)
0.861 (0.208-1.748)
76.205 (11.008-539200188.2)
0.658 ± 0.248
2.656
0.437
0.008
0.933

Oleic Acid
0.193 (0.023-0.374)
0.949 (0.507-4.200)
46.831 (7.483-203445.94)
0.757 ± 0.251
3.019
0.282
0.003
0.963

Stearic acid
0.180 (0.058-0.302)
0.564 (0.345-0.974)
9.224 (3.379-174.164)
1.056 ± 0.256
4.118
1.306
0
0.728

Soybean oil
0.025 (0.013-0.035)
0.051(0.037-0.077)
0.298(0.156-1.421)
1.676 ± 0.376
4.454
0.294
0
0.863

Topical spray method

Palmitic acid
0.667 (0.082-191865.849)
11.922 (2.231-2.078E+46)
2008.321 (32.566-4.743E+195)
0.519 ± 0.260
1.996
0.045
0.046
0.997

Oleic Acid
0.465
5.336
2070.177
0.495 ± 0.255
1.941
0.885
0.052
0.829

Stearic acid
0.442 (0.364-0.526)
1.464(1.178-1.941)
27.361(6.890-1916.773)
1.008 ± 0.268
3.762
1.369
0
0.713

Soybean oil
0.031 (0.015-0.046)
0.074 (0.050-0.155)
0.615 (0.239-11.449)
1.389±0.373
3.725
0.755
0
0.685

Note: The concentrations were obtained using 2%, 1%, 0.5%, 0.25%, and 0.125% solutions except 0.12%, 0.06%, 0.03%, and 0.0125% for Soyabean Oil.

Fig. 1

Lethal time (LT₅₀) ratio between the leaf dip method and topical spray method of exposure to soybean oil and fatty acids at different concentrations of each treatment over observational time (24 h, 48h, 72h, and 96h) against Panonychus citri and its predators.

Fig. 2

Lethal time (LT₅₀) ratio between the leaf dip method and topical spray method of exposure to soybean oil and fatty acids at a lethal concentration of each treatment over observational time (4 h, 8 h, 12 h, 24 h, 48 h, 72 h, and 96 h) against Panonychus citri and its predators.

Table 2

The lethal efficacy of soybean and fatty acids against Panonychus citri and its predators was exposed using leaf dip and topical spray after 24 h of exposure.

Treatments
Leaf dip method
Topical Spray method

Mortality %
Total no. eggs
Mortality %
Total no. eggs

Panonychus citri (McGregor) (n=30)

Soybean oil
46.25 ± 0.983a
27.5 ± 0.567b
43.75 ± 0.983a
29.5 ± 0.567b

Palmitic acid
32.917 ± 1.598c
30.75 ± 1.319b
39.583 ± 1.598ab
29.75 ± 1.319b

Oleic acid
50.833 ± 1.22a
27 ± 1.604b
29.583 ± 1.327c
26 ± 1.604b

Stearic acid
38.333 ± 0.63b
30.75 ± 1.319b
35 ± 0.63b
27.75 ± 1.319b

Control
5 ± 1.409d
79.625 ± 2.146a
2.5 ± 1.045d
95 ± 2.557a

Statistics at df = 4,35
F = 218.54, P = <.001
F = 234.83, P = <.001
F = 196.12, P = <.001
F = 345.99, P = <.001

Neoseiulus californicus (McGregor) (n=15)

Soybean oil
0.833 ± 0.833b
12.375 ± 0.905b
0.833 ± 0.833a
14.375 ± 0.905b

Palmitic acid
4.167 ± 1.22a
8.25 ± 0.62c
0.833 ± 0.833a
6.25 ± 0.62d

Oleic acid
0 ± 0b
12.125 ± 0.666b
0 ± 0a
10.125 ± 0.666c

Stearic acid
0 ± 0b
19.875 ± 1.043a
2.5 ± 1.754a
17.875 ± 1.043ab

Control
0 ± 0b
21.875 ± 1.043a
0 ± 0a
19.875 ± 1.043a

Statistics at df = 4,35
F = 7.48, P = <.001
F = 43.08, P = <.001
F = 1.17, P =0.342
F = 40.66, P = <.001

Neoseiulus barkeri Hughes (n=15)

Soybean oil
2.5 ± 1.22ab
7.125 ± 0.833c
3.33 ± 1.26bc
7.625 ± 0.73c

Palmitic acid
5.833 ± 1.511a
5.25 ± 0.62c
7.5 ± 0.833a
11.125 ± 0.693c

Oleic acid
1.667 ± 1.091ab
7.625 ± 0.73c
4.167 ± 1.22ab
7.625 ± 0.73c

Stearic acid
1.667 ± 1.091ab
17.875 ± 1.043b
5 ± 1.091ab
15.875 ± 1.043b

Control
0 ± 0b
27.25 ± 1.77a
0 ± 0c
25.25 ± 1.77a

Statistics at df = 4,35
F = 3.78, P = 0.012
F = 75.07, P = <.001
F = 7.49, P = <.001
F = 47.33, P = <.001

Fig. 3

The lethal efficacy of soybean and fatty acids impact egg hatching percentage and the percentage of hatched eggs reached adultery when exposed to the parental population of Panonychus citri and its predators using leaf dip and topical spray methods.

Table 3

The numbers of female Panonychus citri attracted to, and the numbers of eggs oviposit on the citrus leaves treated (LC50) or untreated with soybean oil and its fatty acids in choice tests.

Treatments
% adults movement
Total no. of eggs

Treated
Untreated
t-value
P-value
Treated
Untreated
t-value
P-value

Panonychus citri (McGregor) (n=30)

Soybean oil
46.667 ± 3.6
53.33 ± 3.6
-1.309
0.238
30.5 ± 2.466
62.25 ± 4.385
-6.311
<.001

Palmitic acid
40.833 ± 2.097
58.33 ± 2.152
-5.824
0.001
21.75 ± 2.213
42.75 ± 2.357
-5.797
0.001

Oleic acid
46.667 ± 2.357
53.33 ± 2.357
-2
0.092
18.25 ± 1.25
44.50 ± 3.50
-7.063
<.001

Stearic acid
41.667 ± 4.41
58.33 ± 4.41
-2.673
0.037
34.75 ± 1.377
54.50 ± 4.173
-4.494
0.004

Table 4

The numbers of female Neoseiulus californicus (McGregor) and Neoseiulus barkeri Hughes attracted to, and the numbers of eggs oviposition on the citrus leaves treated (LC50) or untreated with soybean oil and its fatty acids in choice tests.

Treatments
% adults movement
% prey consumption
Total no. of eggs

Treated
Untreated
t-value
P-value
Treated
Untreated
t-value
P-value
Treated
Untreated
t-value
P-value

Neoseiulus californicus (McGregor) (n=10)

Soybean oil
22.5 ± 4.787
65 ± 6.455
-5.288
0.002
13.75 ± 6.575
43.75 ± 4.27
-3.827
0.009
3.5 ± 0.645
6.00 ± 0.408
-3.273
0.017

Palmitic acid
45 ± 6.455
50 ± 7.071
-0.522
0.62
27.5 ± 3.277
53.75 ± 5.154
-4.317
0.005
5.00 ± 0.707
9.75 ± 1.031
-3.8
0.009

Oleic acid
27.5 ± 4.787
65.00 ± 6.455
-4.666
0.003
15.00 ± 2.041
58.75 ± 6.25
-6.654
<.001
0.75 ± 0.479
5.5 ± 0.645
-5.911
0.001

Stearic acid
45.00 ± 6.455
55.00 ± 6.455
-1.095
0.315
25.00 ± 2.041
51.25 ± 5.543
-4.444
0.004
4.75 ± 0.629
12.25 ± 0.946
-6.599
<.001

Neoseiulus barkeri Hughes (n=10)

Soybean oil
37.5 ± 4.787
60 ± 4.082
-3.576
0.012
23.75 ± 3.75
48.75 ± 5.543
-3.735
0.01
1.50 ± 0.289
8.75 ± 0.854
-8.043
<.001

Palmitic acid
45.00 ± 2.887
47.5 ± 4.787
-0.447
0.67
15.00 ± 2.041
40.00 ± 2.041
-8.66
<.001
2.00 ± 0.707
5.75 ± 0.479
-4.392
0.005

Oleic acid
22.5 ± 6.292
75.00 ± 6.455
-5.824
0.001
16.25 ± 3.75
56.25 ± 4.27
-7.039
<.001
0.75 ± 0.479
3.50 ± 0.645
-3.422
0.014

Stearic acid
40.00 ± 4.082
60.00 ± 4.082
-3.464
0.013
28.75 ± 2.394
58.75 ± 2.394
-8.863
<.001
4.00 ± 0.913
6.00 ± 1.08
-1.414
0.207