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Article

Evaluation of Bioinseticide in the Control of Plutella xylostella (Linnaeus, 1758): A Laboratory Study for Large-Scale Implementation

by
Silvana Aparecida de Souza
1,
Isabella Maria Pompeu Monteiro Padial
2,
Thais Silva de Souza
3,
Alberto Domingues
2,
Eliana Aparecida Ferreira
1,
Munir Mauad
2,
Claudia Andrea Lima Cardoso
4,
José Bruno Malaquias
5,
Luana Vitória de Queiroz Oliveira
5,
Anelise Samara Nazari Formagio
6,
Juliana Rosa Carrijo Mauad
3 and
Rosilda Mara Mussury
1,6,*
1
Postgraduate Program in Entomology and Biodiversity Conservation, Faculty of Biological and Environmental Sciences, Federal University of Grande Dourados, Dourados Highway-Itahum, km 12, Dourados 79804-970, MS, Brazil
2
Faculty of Agricultural Sciences, Federal University of Grande Dourados, Highway Dourados-Itahum, km 12, Dourados 79804-970, MS, Brazil
3
Faculty of Biological and Environmental Sciences, Federal University of Grande Dourados, Highway Dourados-Itahum, km 12, Dourados 79804-970, MS, Brazil
4
Center of Studies in Natural Resources, State University of Mato Grosso do Sul, Highway Doura-dos-Itahum, km 12, Dourados 79804-970, MS, Brazil
5
Entomology Laboratory, Agrarian Science Center, Joao Pessoa 58397-000, PB, Brazil
6
Postgraduate Program in Biodiversity and Environmental, Faculty of Biological and Environmental Sciences, Federal University of Grande Dourados, Dourados Highway-Itahum, km 12, Dourados 79804-970, MS, Brazil
*
Author to whom correspondence should be addressed.
Sustainability 2025, 17(4), 1626; https://doi.org/10.3390/su17041626
Submission received: 23 December 2024 / Revised: 11 February 2025 / Accepted: 12 February 2025 / Published: 15 February 2025
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Abstract

:
Plutella xylostella is the primary lepidopteran pest of Brassica crops due to its resistance to numerous insecticides. Multipesticide resistance in insects of agricultural importance is a global problem, and new methods of effective control that are less harmful to the environment are becoming increasingly necessary. The present study analyzed the effects of the aqueous extract of Simarouba sp. at concentrations of 10, 5, 1 and 0.1% in comparison with distilled water (as a control) on the feeding preference, oviposition, and embryonic development of P. xylostella. The results demonstrated that the aqueous extract of Simarouba sp. decreased oviposition and feeding in P. xylostella. A reduction in larval hatching was also observed, indicating ovicidal properties. In particular, the 1% concentration resulted in a more significant decrease in oviposition and the number of hatched larvae. Furthermore, concentrations of 10% and 5% caused food intake suppression, while concentrations of 1% and 0.1% reduced dietary intake by 97% and 78%, respectively. This study highlights the efficacy of Simarouba sp. aqueous extract in controlling the diamondback moth, as larval feeding and the number of individuals reaching the larval stage were reduced. Thus, the control method used in this laboratory study is expected to be successful if utilized on a large scale.

1. Introduction

Using insecticides of plant origin to control insect pests is an ancient practice that has persisted for centuries [1]. In China, Egypt, Greece, and India, botanical insecticides remained the primary management method for at least two millennia [2,3,4]. However, since World War II, synthetic insecticides have been widely used to control insect pests. The application of synthetic insecticides on crops has allowed for an increase in agricultural activity and, consequently, in production [5]. However, indiscriminate and inappropriate pesticide usage has resulted in the death of pollinators, such as bees and butterflies [6,7,8], and natural enemies of pest species [9,10]. Further, it may lead to the emergence of more resistant insects [11,12].
Plutella xylostella (Linnaeus, 1758) (Lepidoptera: Plutellidae), popularly known as the diamondback moth, is a cosmopolitan insect that feeds on plants belonging to the family Brassicaceae [13]. Due to its high reproductive potential and short life cycle [14], P. xylostella has become one of the main crop pests worldwide. The combination of these factors and inadequate control strategies have contributed to the development of resistance in the diamondback moth to all the main classes of registered insecticides [15,16].
Botanical insecticides have reemerged as an alternative to chemical control [17] since, generally, they do not favor the evolution of resistance in herbivorous insects [18,19], and are less likely to be toxic to soil, water, and nontarget organisms, such as natural predators, pollinators, vertebrates [20], and invertebrates [21]. In addition, they are both low cost and easy to acquire, apply, and manage [22].
Botanical insecticides have multiple modes of action and do not always act as biocides [21]. These specific characteristics of plant-based insecticides are essential for integrated pest management in that, even if they do not cause the immediate death of insects, they can exert sublethal effects, such as phagodeterrence, ovideterrence [23,24], reduction in the weight of immature insects, reduction in fertility and fecundity, and changes in insect development [21], significantly reducing pest populations and decreasing the damage caused to crops. In addition to all of these factors, due to the ease of obtaining and applying botanical insecticides [22], they have become a viable alternative for small farmers [17]. Therefore, botanical insecticides play a vital role in the search for safer and more balanced strategies for controlling agricultural pests.
The Simaroubaceae family comprises 32 genera and more than 170 species [23]. In Brazil, this family presents six genera: Simaba and Simarouba, present throughout the country; Castela and Picrasma, located in the South; and Quassia and Picrolemma, predominant in the Amazon [24]. Simarouba is a medium-sized tree, reaching up to 20 m in height, with a trunk that varies between 50 and 80 cm in diameter. It has shiny green leaves that are 20 to 50 cm long, small white flowers, and small red fruits [25,26].
Previous studies on Simarouba genus members have identified the presence of numerous bioactive compounds, such as alkaloids, quassinoids [23], triterpenes, and flavonoids [25], which can act as antifeedant substances [27,28] or interfere with the physiology of insect pests [29,30,31]. In the central region of Mato Grosso do Sul, Brazil (where this study was carried out), the Simarouba species was selected due to observations made on site, in which the absence of insect presence or attacks on the plant was noted.
In practical terms, we believe that this simulated practice enables future prospecting with respect to the effectiveness of this botanical insecticide in the field, bringing quality food production to communities and creating new prospects for sustainable rural development in line with sustainable development goals. Considering the importance of Brassica cultivation and the use of aqueous extract in integrated pest management, our objective was to evaluate the effects of the aqueous extract made from Simarouba sp. at different concentration levels on the feeding, oviposition and embryonic development of P. xylostella. The results may support future control planning of this pest using an aqueous extract of Simarouba sp. as a rapid, low-cost insecticide, enabling effective population control. Thus, we aimed to answer the following questions: What is the feeding and oviposition preference of P. xylostella when allowed to choose the substrate? Is embryonic development compromised?

2. Materials and Methods

The experiments and the rearing of insects were performed in the Laboratory of Insect–Plant Interactions, School of Biological and Environmental Sciences, Federal University of Grande Dourados (UFGD), Mato Grosso do Sul, Brazil. The insects were kept at a constant temperature (25 ± 2 °C) and relative humidity (70 ± 5%) with a photoperiod of 12 h.

2.1. Insects

The P. xylostella stock was established using individuals collected from the Brassica oleracea var. acephala organic gardens in Itaporã, Mato Grosso do Sul, Brazil. The P. xylostella rearing methodology was adapted from Barros et al. [32].
The diamondback moth pupae were transferred to plastic cages (9 cm × 19 cm × 19 cm) until the moths emerged. The adults were fed with a solution of honey diluted in 10% distilled water. We used organic cabbage discs (Brassica oleracea var. acephala) and filter paper moistened with distilled water (measuring 9 cm Ø) as oviposition substrates. We then transferred the oviposited discs to new plastic containers (30 cm × 15 cm × 12 cm). After the eggs hatched, P. xylostella larvae remained in these plastic containers until they reached the pupal stage. The larvae were fed organic cabbage leaves that had been previously disinfected with 5% sodium hypochlorite. We sanitized the cages and replaced the cabbage leaves every 48 h. Pupae were transferred back to the adult cage, and the cycle started again.

2.2. Aqueous Extract of Simarouba sp.

We collected leaves of fully expanded Simarouba sp. from an area dominated by Cerrado in Campo Grande, Mato Grosso do Sul, Brazil (latitude: 21°13′28″ S, longitude: 54°11′28″ W; altitude: 437 m). The National Council of Brazilian Research (CNPq) authorized the collection of botanical material under permit number AF5E2AA for the Management of Genetic Heritage (CGEN/MMA).
We washed the Simarouba sp. leaves (380 g) under running water, dried them in an oven (AC-035/81) with forced circulating air at 45 ± 3 °C for 72 h, pulverized them using a Willey knife mill, and sieved them through a 10 mm mesh (MA340/A). The resulting powder (86 g) was stored in plastic containers to protect it from moisture and light. We used part of the powdered material to obtain an aqueous extract (AE-S) from Simarouba sp., with concentrations of 10, 5, 1, and 0.1%, for use as an aqueous extract, as follows: (i) 3 g of the powder in 30 mL of distilled water, (ii) 1.5 g in 30 mL, (iii) 0.3 g in 30 mL, and (iv) 0.015 g in 30 mL, respectively. All AE-S were refrigerated for 24 h and subsequently filtered using filter paper.

2.3. Effect of Aqueous Extract on the Food Preference of P. xylostella in a Free-Choice Test

We immersed discs of organic cabbage (Brassica oleracea var. acephala) with 4 cm Ø in the AE-S at concentrations of 10, 5, 1 and 0.1%. We then placed them on filter paper for approximately 40 min to allow the solution to dry. The control consisted of discs immersed in distilled water.
Subsequently, we transferred four cabbage discs to a Petri dish (9 cm in diameter and 1.5 cm in height). We placed the discs across from and equidistant to each other, with two discs immersed in the AE-S and the other two in water (i.e., the control). Then, the third instar stock-reared P. xylostella larvae were released onto the center of the dish. The larvae remained on the Petri dish for 24 h, possibly choosing between discs treated with AE-S or control discs.
After 24 h, the cabbage discs were removed and scanned (Figure 1), the leaf area consumed was measured using ImageJ software (1.54m 5 December 2024), and Kogan and Goeden’s food preference index (FPI) of Kogan and Goeden was calculated [33]. We calculated FPI through the consumed leaf area using the following formula: FPI = 2A/(M + A), where A is the consumed area of the treated discs, and M is the consumed area of the untreated discs. We obtained an index between 0 and 2. The extract was classified as a phagostimulant, neutral, or a phagodeterrent. It was classified as a phagostimulant if the index was greater than 1, as neutral if it was equal to 1, and as a phagodeterrent if it was lower than 1.

2.4. Effect of Aqueous Extract on the Oviposition of P. xylostella in a Free-Choice Test

Stock-reared pupae were kept in individual test tubes until adult emergence. The sex of the moths was determined based on the sexual dimorphism of the adults [34], and couples were formed.
Subsequently, we immersed 4 cm Ø cabbage discs in AE-S at concentrations of 0.1, 1, 5, and 10%. Control discs were immersed in distilled water. We placed the discs on sheets of filter paper for approximately 40 min to allow the liquid to dry. Then, couples consisting of adults up to 12 h postemergence were placed in plastic cages, with one couple per cage (8 cm diameter × 6 cm height), where they remained for 10 days. After that time, we evaluated oviposition preference based on the oviposition preference index (OPI) described by Kogan and Goeden [33].
A moistened filter paper disc measuring 8 cm Ø and four cabbage discs measuring 4 cm Ø (two control discs immersed in water and two discs immersed in the AE-S) were added to each cage as oviposition substrates. We changed the discs every 24 h and counted the number of eggs on the discs. Cotton soaked in a honey solution diluted in 10% distilled water was offered as food (Figure 2).
The effect of AE-S on the oviposition of diamondback moths was evaluated using the oviposition preference index (OPI) described by Kogan and Goeden [33]. It was calculated through the formula OPI = 2A/(M + A), where A is the number of eggs on the leaves immersed in the extract and M is the number of eggs on the leaves immersed in distilled water. The OPI values range from 0 to 2, with values greater than 1 leading to classification as an ovistimulant, values equal to 1 leading to classification as neutral, and values less than 1 leading to classification as an ovideterrent.

2.5. Effects of Aqueous Extract on the Embryonic Phase of P. xylostella

Stock-reared P. xylostella pupae were kept in individual test tubes until adult emergence. After the emergence and sexing of adults, we released two couples (up to 12 h old) into transparent plastic cages (8 cm diameter × 6 cm height) containing three cabbage discs (4 cm Ø) on filter paper discs (8 cm Ø), which were used as oviposition substrates.
After 24 h, the discs on which the insects oviposited were removed and carefully cut into smaller areas, each containing 10 eggs [35]. Then, we immersed these eggs in AE-S at concentrations of 10, 5, 1, and 0.1% for 30 s and transferred them individually to Petri dishes. The control consisted of distilled water. The number of hatched larvae was counted daily (Figure 3) and compared with the number of eggs with a transparent chorion using a stereoscopic magnifying glass @BelSZLed-45x, Monza, Itália.

2.6. Statistical Analysis

2.6.1. Free-Choice Food Preference Experiment

The experiment was conducted using a completely randomized design with 30 replicates. Each replicate consisted of a plate with four discs and one third instar larvae. The data were subjected to an analysis of variance (ANOVA) with a Gaussian distribution, and the means were compared using Student’s t-test with a 5% probability.

2.6.2. Free-Choice Oviposition Experiment

We used a completely randomized experimental design to evaluate oviposition during the free-choice test: 5 treatments (4 concentrations and a control) were used, where each treatment consisted of 10 replicates (i.e., 10 cages). The generalized linear model with a Poisson distribution with overdispersion had the best goodness-of-fit for the number of eggs. The means were compared by the F test (p < 0.05). We assessed the model’s goodness-of-fit with a half-normal plot [35].

2.6.3. Effects of Aqueous Extract on the Embryonic Phase of P. xylostella

The experimental design was completely randomized with 5 treatments (4 concentrations plus control) and 10 replicates, with 10 eggs in each replicate. The generalized linear model with a binomial distribution with overdispersion had the best goodness-of-fit for the number of eggs. The means were compared via the F test (p < 0.05), and the goodness-of-fit of the model was assessed with a half-normal plot [36].

2.7. Chemical Composition

The aqueous extracts (AE-S) obtained according to the methods described in Section 2.2 were lyophilized using the Alpha 1–2LD Plus system under the parameters of a 0.045 mbar vacuum and a temperature of −42 °C. This process produced a 12% yield. The lyophilized aqueous extract was stored at 4 °C and protected from light until further testing. For analysis, the lyophilized aqueous extracts were then solubilized at a concentration of 1 mg/mL. Results were expressed as the average of four extracts prepared in this study, with each sample analyzed in triplicate.

2.7.1. Assessing the Content of Phenolic Compounds by the Folin–Ciocalteu Method

First, 0.5 mL of Folin–Ciocalteu reagent (1:10 v/v) and 1 mL of distilled water were added to 0.1 mL of the sample and incubated for 1 min. Subsequently, 1.5 mL of 20% sodium carbonate (w/v) was added, and the reaction was allowed to proceed for 2 h in the dark. The sample was then analyzed using a UV–Vis spectrophotometer FEMTO model 700 PLUS, São Paulo, Brazil) at a wavelength of 760 nm [37]. The analysis was performed in triplicate, using distilled water as a blank. For quantification, an analytical curve of gallic acid, subjected to the same chemical reaction as the samples, was used. Results were expressed as gallic acid equivalents (GAEs) in mg/g of lyophilized aqueous extract.

2.7.2. Flavonoid Content Analysis by the Aluminum Chloride Method

Aluminum chloride 2% (1 mL) in methanol was added to 1 mL of the sample, and the reaction was allowed to proceed for 15 min. The sample was analyzed using a UV–Vis spectrophotometer at a wavelength of 430 nm [37]. Distilled water was used as a blank, and the analyses were performed in triplicate. For quantification, an analytical curve was prepared using rutin, and the results were expressed as quercetin equivalents (QEs) in mg/g of lyophilized aqueous extract.

2.7.3. Tannin Content Analysis by the Folin–Denis Method

The tannin content was determined using the Folin–Denis spectrophotometric method described by [38], with modifications applied to the reagent volumes while maintaining the concentrations. To each 0.5 mL of sample, 0.5 mL of Folin–Denis reagent and 0.5 mL of 8% sodium carbonate were added, and the mixture was allowed to react for 120 min. Readings were performed using a spectrophotometer at a wavelength of 725 nm. An analytical curve constructed with a tannic acid standard was used to calculate the tannin concentration. Results were expressed in tannic acid equivalents (TAEs) in mg/g of lyophilized aqueous extract.

2.7.4. DPPH Radical Scavenging Activity

Samples (0.1 mL) were mixed with 3 mL of 0.004% DPPH radical solution and maintained in the dark for 30 min. After this period, the absorbance was measured at a wavelength of 517 nm. The readings were performed in triplicate, with distilled water used as a blank. The percentage of DPPH inhibition (%) was calculated, as described in [39], to determine the minimum inhibitory concentration.

3. Results

3.1. Effect of Aqueous Extract on the Feeding Preference of P. xylostella

The leaf area consumed varied significantly among all AE-S concentrations evaluated (Figure 4). There was no consumption of the discs treated with AE-S at concentrations of 10% and 5% (Table 1). At the 1% concentration, AE-S promoted a reduction in consumption of approximately 97% compared to the control discs. For the 0.1% concentration, the botanical extract promoted a reduction in larval feeding of roughly 78% compared to the control (Table 1).
According to the food preference index, all AE-S concentrations were classified as phagodeterrents; that is, the AE-S-treated discs reduced the food intake of P. xylostella (Table 1).

3.2. Effect of Aqueous Extract on P. xylostella Oviposition

The results showed that all AE-S concentrations significantly affected the fecundity of P. xylostella. Regarding the daily mean oviposition, we observed that females showed a pattern of recognition for the treated discs for up to 3 days, except for the 5% AE-S group; after this period, there were drastic decreases in oviposition on discs treated with the aqueous extract (Figure 5).
At the 10% and 5% concentrations, oviposition was absent on days 8 and 9, respectively. However, at the 1% and 0.1% concentrations, the absence of oviposition occurred only on the last day of evaluation (Figure 5).
The 10% AE-S concentration caused an average reduction of 47.50 eggs/couple; that is, a reduction of approximately 66% (Figure 6). Notably, the observations were made over 10 days; the females that had contact with the AE-S at a concentration of 10% died after 8 days, while the males who had received the same treatment remained alive throughout the 10 days. Mortality among the females may have occurred as the females came into direct contact with the oviposition substrate treated with AE-S.
Furthermore, the 5% AE-S concentration reduced the total number of eggs by approximately 62% compared to the control. In addition, the 1% and 0.1% AE-S concentrations reduced oviposition by 60% compared to the control, with mean reductions of 66.50 and 80 eggs per couple, respectively (Table 2).
The oviposition preference index (OPI) demonstrated the insects’ preference for the untreated substrate (control) and a slight preference for substrates treated with AE-S. Thus, the aqueous extract was classified as an ovideterrent (Table 2). Note that all AE-S concentrations interfered with the choice of P. xylostella females for treated discs, resulting in lower oviposition rates. None of the concentrations suppressed oviposition; however, there was a substantial reduction in the number of eggs oviposited on the discs. Treatment with AE-S resulted in a mean decrease in oviposition by P. xylostella of 63.62% (Table 2).

3.3. Effects of Aqueous Extract on the Embryonic Phase of P. xylostella

The aqueous extract of Simarouba sp. affected the embryonic development of P. xylostella eggs at all concentrations, reducing the number of hatched larvae (F = 4.85; df = 4; p = 0.0027; CV = 8.93) and showing ovicidal properties (Table 3). The 1% AE-S concentration affected larval hatching the most, reducing the number of hatched larvae by 28.42% on average, when compared to the control. However, this treatment did not significantly differ from the other concentrations, with the 10%, 5% and 0.1% AE-S concentrations reducing the hatching of diamondback moth eggs by 23.62%, 20.70%, and 13.21% on average, respectively, compared to the control (Table 3).
In general, all the concentrations reduced the number of hatched larvae by an average of 21.48%. In addition, there were no significant differences among the AE-S concentrations, which indicates that any of the concentrations used will affect the hatching of P. xylostella eggs (Table 3).
Analysis of the lyophilized aqueous extract of Simarouba sp. indicated the presence of phenolic compounds (354.13 ± 2.04 mg GAE/g extract), flavonoids (247.11 ± 5.43 mg QE/g extract), and condensed tannins (52.11 ± 0.43 mg TAE/g extract). This extract also demonstrated effective radical cation scavenging activity (DPPH), with a minimum inhibitory concentration of 87.31 ± 2.32 µg/mL.

4. Discussion

4.1. Feeding

Our results showed that the aqueous extract of Simarouba sp. can be used as a botanical insecticide that effectively controls P. xylostella, affecting its feeding, oviposition, and embryonic development.
Insects use a complex and specialized chemosensory system to find their mates, locate food sources, identify suitable sites for laying eggs, avoid dangerous situations, and identify unsuitable habitats and hosts [40,41]. However, secondary plant metabolites can alter the choice and acceptance of the host [42], making substrates unpleasant or less attractive due to a bad smell or bitter taste [43,44].
We observed that, at concentrations of 10% and 5%, the AE-S prevented the onset of feeding by P. xylostella larvae, causing them to feed only on untreated discs (control). De Souza et al. [21] observed the same behavior in first instar larvae of P. xylostella exposed to cabbage discs treated with AE-S at concentrations of 10% and 5%. We also observed that the larvae that fed on the discs treated with AE-S exhibited reduced mobility.
At the lowest concentrations (1% and 0.10%), the larvae took a test bite and initially fed on the treated discs, which led to changes in the physiological mechanisms of the insects. The chemosensory system of insects comprises olfactory and gustatory systems [45]. The gustatory system relies on complex proteins found in the antennae, maxillary palps, lips, legs, and genitals [46] to detect significantly non-volatile chemical compounds, such as amino acids, sugars, and compounds with a bitter taste [47,48]. Compared with the control, the lowest concentrations reduced intake by an average of 87.3% (Table 1).
Given our findings, we concluded that, although P. xylostella feeds voraciously—especially in the third and fourth instars [49]—the reduction in larval feeding on Brassicaceae is extremely important from the viewpoint of pest control. This is because the lower consumption of leaves suggests a decrease in damage and, consequently, a reduction in losses for the farmer.
During the larval stage, insects must ingest a sufficient amount of nutrients to be converted into growth tissue [50]. Thus, swallowing AE-S at all concentrations compromises larval feeding and may cause sublethal effects throughout the insect’s life cycle, as was observed by de Souza et al. [21] when evaluating the effect of AE-S at different concentrations on the biology of P. xylostella. They observed that AE-S promoted a mortality greater than 70% in the larval stage, reduced pupal biomass by approximately 33%, affected development at metamorphosis, and promoted low fertility in adults [21].

4.2. Oviposition

AE-S affected the oviposition preference of P. xylostella, with a mean reduction of 64% in the number of eggs deposited on the treated discs. In addition, AE-S reduced the number of hatched larvae by 21% on average. Arthropods use chemical, physical, and/or morphological stimuli [51] to choose the substrate on which they lay eggs. These stimuli are observed through vision, smell, touch, and taste [42]. Plant extracts contain antixenotic substances that can confuse females during the plant selection process, especially in the evaluation and acceptance phase [52], making substrates containing such substances less-used for oviposition [53]. In particular, due to their nocturnal habit [15], females may be guided by the identification of odors.
In particular, P. xylostella uses its antennae and abdominal segments to feel the substrate and verify whether it is safe for laying eggs [54,55,56]. The antennae play a crucial role in the detection of odorous substances via odorant receptors (ORs) that work together with odorant proteins (OPs) and other chemosensory proteins (CSPs) to identify these substances [57]. A study by Engostia et al. [58] identified the presence of 95 ORs in P. xylostella. Thus, we believe that the reduction in the number of eggs in the treated discs was due to the presence of volatile compounds in the AE-S, causing repellent action or irritability among females when in contact with the treated substrate.
Daily fluctuations in the number of eggs produced by P. xylostella couples under the different treatments were observed. Starting on the third day of oviposition, there was a reduction in the number of eggs in all treatments—including the control—suggesting the possibility of the AE-S spreading throughout the cages and interfering with oviposition preference even in the control treatment. Under normal conditions, a P. xylostella female lays an average of 160 eggs but can lay up to 300 [15]. As the test included a choice of substrates, the possibility of the extract interfering with the selection of substrates for oviposition should be considered, although this possibility was not evaluated.

4.3. Embryonic Development

The death of the embryos—and, consequently, the reduction in the hatching of eggs—may have been caused by the penetration of AE-S through micropores on the eggs. These micropores are approximately 0.8 mm in size and allow for gas exchange within the egg [35]. In addition, the eggs of P. xylostella have rough chorions, facilitating the penetration of the extract into eggs [35]. In this sense, reducing the number of eggs and eggs hatching on treated discs after contact with AE-S can result in a future reduction in the population, consequently decreasing the losses and costs associated with the management of P. xylostella [59]. In addition, AE-S reduced the number of individuals reaching the larval stage, especially the first stage, in which the larvae have a mining habit, feeding on the leaf parenchyma [60]. This behavior prevents the larvae from coming into contact with insecticides, making pest control difficult.

4.4. Chemical Composition

We believe that phenolic compounds, tannins, flavonoids [25,61,62], alkaloids, and quassinoids (e.g., 11-acetylamarolide, ailanthinone, and glaucarubinone) [21] present in the aqueous extract of Simarouba sp. may be responsible for the changes observed in P. xylostella.
Alkaloids are secondary metabolites that act on the nervous system of insects [63]. They may interfere with neuroendocrine control by inactivating acetylcholinesterase in larvae, causing neurotoxicity [64,65]. These compounds have adulticidal action; that is, they cause adult mortality [66].
Flavonoids can directly affect reproduction, and have been shown to decrease the oviposition of Callosobruchus chinensis (L.) (Coleoptera: Bruchidae) and P. xylostella [67,68] and reduce egg hatching [69]. Ferreira et al. [70] observed a 90% reduction in oviposition when they exposed P. xylostella females to an aqueous extract of Ludwigia spp. (Onagraceae). In addition, it has been observed that an aqueous extract of L. tomentosa reduced leaf consumption in 81% of the third instar larvae of P. xylostella. In the phytochemical analysis, the authors observed that the obtained aqueous extract contained phenolic compounds, flavonoids, condensed tannins, and alkaloids—substances capable of affecting the feeding and oviposition of insects. In a recent study, Padial et al. [71] found that an aqueous extract of leaves of Miconia albicans (Sw.) Triana (Melastomataceae) promoted a 78% reduction in feeding and a 94% reduction in the oviposition of diamondback moths. The authors explained that the phagodeterrent and ovideterrent effects were due to the presence of phenolic compounds, flavonoids, and tannins.
Quassinoids can be classified as taxonomic markers of Simaroubaceae, as they are synthesized almost exclusively by members of this family [23,24]. Previous studies have indicated that quassinoids can inhibit feeding through activating systems that identify substances with a bitter taste [27,28,72]; this finding was confirmed in the present study. A bitter taste is commonly associated with toxic substances that cause aversive responses in insects [69]. Thus, the recognition of bitter compounds is an essential ability for insects, mainly due to the diversity and toxicity of these compounds [69,73].
Different quassinoids have been identified as insect-feeding and -growth regulator agents in the literature [74]. Previous studies have shown the insecticidal activities of quassinoids against Tetranychus urticae (koch, 1936) (acari: tetranychidae), Myzus persicae Sulz. (Hemiptera: Aphididae), Meloidogyne incognita [75], and Rhodnius milesi (Carcavallo et al., 2001) (Hemiptera:Triatominae) [76]. Further, they also have shown anti-feeding potential against Locusta migratoria migratorioides (Reiche and Fairmaire, 1849) (Orthoptera, Acrididae) [77] and other agricultural pests [78]. Specifically, quassin, simalikalactone D, bruceantin, glaucarubinone, and isobrucein demonstrated significant feeding deterrence against the Mexican bean beetle (Epilachna varivestis Mulsant (Coleoptera:Coccinellidae)) and the diamondback moth (P. xylostella) [79].
The results presented by Polonsky et al. [80] reinforce the potential of quassinoides as insect-feeding deterrent agents. Among the identified compounds, isobrucein A, isobrucein B, brucein B and C, glaucarubinone, and quassin significantly reduced Myzus persicae (Hemiptera, Aphididae) feeding at concentrations of 0.05% and 0.01%.
As a proposal for further research, we strongly believe that field tests with this species should be carried out, evaluating the productivity of vegetables based on insect control through the use of aqueous extracts (or botanical insecticides), thus ensuring the adoption of sustainable agricultural practices, the preservation of natural ecosystems and the mitigation of environmental impacts. This represents a substantial contribution to the local bioeconomy, primarily through access to high-value markets, such as the healthy and sustainable food market.

5. Conclusions

Our study identified that the aqueous extracts of Simarouba sp. compromised embryonic development, significantly reduced feeding and oviposition preference, and at higher concentrations, ultimately prevented feeding by P. xylostella. Our initial laboratory studies demonstrated that this plant has great potential for use on a large scale. However, further studies must be conducted to ensure its economic viability and determine its toxicity in the environment and in humans.

Author Contributions

Conceptualization, S.A.d.S. and R.M.M.; methodology, S.A.d.S., R.M.M., C.A.L.C. and J.B.M.; software, S.A.d.S., R.M.M. and J.B.M.; validation, S.A.d.S., R.M.M. and J.B.M.; formal analysis, S.A.d.S., R.M.M., J.B.M., C.A.L.C. and A.S.N.F.; investigation, S.A.d.S., R.M.M., J.B.M., I.M.P.M.P., T.S.d.S., A.S.N.F., A.D., E.A.F., M.M., C.A.L.C., L.V.d.Q.O., A.S.N.F. and J.R.C.M.; resources, S.A.d.S., R.M.M. and J.B.M.; data curation, S.A.d.S., R.M.M. and J.B.M.; writing—original draft preparation, S.A.d.S., R.M.M., J.B.M., I.M.P.M.P., T.S.d.S., A.S.N.F., E.A.F., M.M., C.A.L.C., A.S.N.F. and J.R.C.M.; writing—review and editing, S.A.d.S., R.M.M., J.B.M., J.R.C.M. and M.M.; supervision, S.A.d.S. and R.M.M.; project administration, R.M.M. All authors have read and agreed to the published version of the manuscript.

Funding

This study was funded by Fundação de Apoio ao Desenvolvimento do Ensino, Ciência e Tecnologia do Estado de Mato Grosso do Sul (FUNDECT), and the resources were provided under grant no. 83/029.649/2024 and by the National Council of Brazilian Research (CNPq).

Institutional Review Board Statement

The National Council of Brazilian Research (CNPq)/Council for the Management of Genetic Heritage (CGEN/MMA) authorized the collection of the botanical material under permit number AF5E2AA.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data are contained within the article.

Acknowledgments

The authors thank the National Council for the Improvement of Higher Education (CAPES), Brazil, for providing a scholarship to the first author, the National Council for Scientific and Technological Development (CNPq) for the last researcher’s productivity scholarship, and the FUNDECT’s financial support for research; Itaipu Binacional and Itaipu Parquetec.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Schematic representation tof the methodology used to evaluate the effect of AE-S on the feeding preference of P. xylostella.
Figure 1. Schematic representation tof the methodology used to evaluate the effect of AE-S on the feeding preference of P. xylostella.
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Figure 2. Schematic representation of the methodology used to evaluate the effect of AE-S on the oviposition preference of P. xylostella.
Figure 2. Schematic representation of the methodology used to evaluate the effect of AE-S on the oviposition preference of P. xylostella.
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Figure 3. Schematic representation tof the methodology used to evaluate the effect of AE-S on the embryonic phase of Plutella xylostella.
Figure 3. Schematic representation tof the methodology used to evaluate the effect of AE-S on the embryonic phase of Plutella xylostella.
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Figure 4. Leaf area consumed (±SE) and food preference index of Plutella xylostella exposed to cabbage discs treated with a Simarouba sp. bioinsecticide at different concentrations. All grouped bars (control versus concentration) differ significantly according to Student’s t-test at a 5% probability level. The preference index was calculated at 0.11, 0.01, 0.00, and 0.00 to the concentrations of 0.01, 1, 5, and 10%, respectively. Thus, all concentrations were classified as phagodeterrent according to Kogan and Goeden [33,36].
Figure 4. Leaf area consumed (±SE) and food preference index of Plutella xylostella exposed to cabbage discs treated with a Simarouba sp. bioinsecticide at different concentrations. All grouped bars (control versus concentration) differ significantly according to Student’s t-test at a 5% probability level. The preference index was calculated at 0.11, 0.01, 0.00, and 0.00 to the concentrations of 0.01, 1, 5, and 10%, respectively. Thus, all concentrations were classified as phagodeterrent according to Kogan and Goeden [33,36].
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Figure 5. Mean number of Plutella xylostella eggs over 10 days during the oviposition preference experiment using cabbage discs treated with aqueous extract of Simarouba sp. at different concentrations: (A) 10%; (B) 5%; (C) 1%; (D) 0.1%.
Figure 5. Mean number of Plutella xylostella eggs over 10 days during the oviposition preference experiment using cabbage discs treated with aqueous extract of Simarouba sp. at different concentrations: (A) 10%; (B) 5%; (C) 1%; (D) 0.1%.
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Figure 6. Number of eggs (±SE) and oviposition preference index of Plutella xylostella on cabbage discs treated with bioinsecticides of Simarouba sp. at different concentrations. Grouped bars (control versus extract) are significantly different when compared by the F test (p < 0.05) using a generalized linear model with a Poisson distribution with overdispersion (quasiPoisson model) at a 5% probability. The preference index was calculated at 0.60, 0.52, 0.55, and 0.60 to the concentrations of 0.01, 1, 5, and 10%, respectively. Thus, all concentrations were classified as ovideterrent according to Kogan and Goeden [33,36].
Figure 6. Number of eggs (±SE) and oviposition preference index of Plutella xylostella on cabbage discs treated with bioinsecticides of Simarouba sp. at different concentrations. Grouped bars (control versus extract) are significantly different when compared by the F test (p < 0.05) using a generalized linear model with a Poisson distribution with overdispersion (quasiPoisson model) at a 5% probability. The preference index was calculated at 0.60, 0.52, 0.55, and 0.60 to the concentrations of 0.01, 1, 5, and 10%, respectively. Thus, all concentrations were classified as ovideterrent according to Kogan and Goeden [33,36].
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Table 1. Leaf area consumed (±SE) and food preference index of Plutella xylostella exposed to cabbage discs treated with an aqueous extract of Simarouba sp. at different concentrations.
Table 1. Leaf area consumed (±SE) and food preference index of Plutella xylostella exposed to cabbage discs treated with an aqueous extract of Simarouba sp. at different concentrations.
Concentration (%)Consumed Leaf Area (cm2)Preference Index 1Classification 1
ExtractControl
100.00 ± 0.00 b
n = 30		0.44 ± 0.03 a
n = 30		0.00Phagodeterrent
50.00 ± 0.00 b
n = 30		0.45 ± 0.03 a
n = 30		0.00Phagodeterrent
10.01 ± 0.00 b
n = 30		0.32 ± 0.03 a
n = 30		0.01Phagodeterrent
0.100.08 ± 0.002 b
n = 30		0.36 ± 0.029 a
n = 30		0.11Phagodeterrent
Means on the line followed by the same letter in a row do not differ significantly according to Student’s t-test at a 5% probability level. 1 According to [33,36].
Table 2. Number of eggs (±SE) and oviposition preference index of Plutella xylostella on cabbage discs treated with Simarouba sp. aqueous extract concentrations.
Table 2. Number of eggs (±SE) and oviposition preference index of Plutella xylostella on cabbage discs treated with Simarouba sp. aqueous extract concentrations.
Concentration (%)Average Number of EggsFpPreference
Index 1		Classification 1
ExtractControl
1028.30 ± 6.08 b
n = 10		60.40 ± 8.57 a
n = 10		=7.7002=0.00510.60Ovideterrent
555.50 ± 1.27 b
n = 10		146.00 ± 7.74 a
n = 10		=196.53<0.00010.55Ovideterrent
147.40 ± 9.53 b
n = 10		119.80 ± 13.27 a
n = 10		=19.127<0.00010.52Ovideterrent
0.1057.00 ± 5.92 b
n = 10		133.50 ± 9.37 a
n = 10		=49.458<0.00010.60Ovideterrent
Means on the line were compared by the F test (p < 0.05) using a generalized linear model with a Poisson distribution with overdispersion (quasiPoisson model) at a 5% probability. 1 According to Kogan and Goeden [33,36].
Table 3. Mean number (±SE) of hatched P. xylostella larvae from eggs exposed to different Simarouba sp. aqueous extract concentrations.
Table 3. Mean number (±SE) of hatched P. xylostella larvae from eggs exposed to different Simarouba sp. aqueous extract concentrations.
Concentrations of Simarouba sp. Aqueous Extract
AE-S 10%AE-S 5%AE-S 1%AE-S 0.1%Control
Number of Hatched Larvae7.63 ± 0.74 b
n = 10		7.92 ± 0.51 b
n = 10		7.15 ± 0.41 b
n = 10		8.67 ± 0.33 ab
n = 10		9.99 ± 0.00 a
n = 10
F and p valueF = 8.94; p < 0.0001
Means on the line were compared by the F test (p < 0.05) using a generalized linear model with a binomial distribution with overdispersion (quasibinomial) at a 5% probability.
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MDPI and ACS Style

Souza, S.A.d.; Padial, I.M.P.M.; Souza, T.S.d.; Domingues, A.; Ferreira, E.A.; Mauad, M.; Cardoso, C.A.L.; Malaquias, J.B.; Oliveira, L.V.d.Q.; Formagio, A.S.N.; et al. Evaluation of Bioinseticide in the Control of Plutella xylostella (Linnaeus, 1758): A Laboratory Study for Large-Scale Implementation. Sustainability 2025, 17, 1626. https://doi.org/10.3390/su17041626

AMA Style

Souza SAd, Padial IMPM, Souza TSd, Domingues A, Ferreira EA, Mauad M, Cardoso CAL, Malaquias JB, Oliveira LVdQ, Formagio ASN, et al. Evaluation of Bioinseticide in the Control of Plutella xylostella (Linnaeus, 1758): A Laboratory Study for Large-Scale Implementation. Sustainability. 2025; 17(4):1626. https://doi.org/10.3390/su17041626

Chicago/Turabian Style

Souza, Silvana Aparecida de, Isabella Maria Pompeu Monteiro Padial, Thais Silva de Souza, Alberto Domingues, Eliana Aparecida Ferreira, Munir Mauad, Claudia Andrea Lima Cardoso, José Bruno Malaquias, Luana Vitória de Queiroz Oliveira, Anelise Samara Nazari Formagio, and et al. 2025. "Evaluation of Bioinseticide in the Control of Plutella xylostella (Linnaeus, 1758): A Laboratory Study for Large-Scale Implementation" Sustainability 17, no. 4: 1626. https://doi.org/10.3390/su17041626

APA Style

Souza, S. A. d., Padial, I. M. P. M., Souza, T. S. d., Domingues, A., Ferreira, E. A., Mauad, M., Cardoso, C. A. L., Malaquias, J. B., Oliveira, L. V. d. Q., Formagio, A. S. N., Mauad, J. R. C., & Mussury, R. M. (2025). Evaluation of Bioinseticide in the Control of Plutella xylostella (Linnaeus, 1758): A Laboratory Study for Large-Scale Implementation. Sustainability, 17(4), 1626. https://doi.org/10.3390/su17041626

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