Insecticidal activity of Psychotria spp., Vatairea spp. and Acosmium spp. on the biological parameters of Plutella xylostella (Linnaeus, 1758) (Plutellidae: Lepidoptera)

Atividade inseticida de Psychotria spp., Vatairea spp. e Acosmium spp. sobre os parâmetros biológicos de Plutella xylostella L. 1758 (Plutellidae: Lepidoptera)

Abstract

In recent years, several botanical species have been tested to determine their ability to reduce the damage caused by Plutella xylostella L. (Lepidoptera: Plutellidae) in brassica crops. Considering the insecticidal potential demonstrated by many botanical species, the effects of the aqueous extracts of Psychotria leiocarpa Cham. & Schltdl, Psychotria deflexa DC., Acosmium subelegans (Mohlenbr.) Yakovlev and Vatairea macrocarpa (Benth.) Ducke by infusion and maceration on the biological parameters of P. xylostella were evaluated. All extracts reduced P. xylostella larval duration and caused larval and egg mortality. In the larvae, the extracts resulted in 70% mortality. In addition, the botanical extracts affected the survival of P. xylostella eggs. The extracts of P. leiocarpa and P. deflexa, prepared by infusion, delayed the emergence of adults, while the extract of V. macrocarpa reduced pupal survival. The longevity of adults was also influenced by the extracts, where the maceration of V. macrocarpa and P. deflexa and infusion of A. subelegans reduced the longevity of P. xylostella females and the maceration of V. macrocarpa and P. leiocarpa reduced the longevity of P. xylostella males. We conclude that the studied extracts were toxic to P. xylostella, especially in the reproduction, of diamondback moth. Consequently, the botanical extracts reduced the number of individuals of the next generation.

Keywords:
diamondback moth; insecticidal plant; Psychotria; Acosmium subelegans; Vatairea macrocarpa

Resumo

Nos últimos anos, várias espécies botânicas foram testadas para determinar sua capacidade de reduzir os danos causados ​​por Plutella xylostella L. (Lepidoptera: Plutellidae) em culturas de brássicas. Considerando o potencial inseticida demonstrado por muitas espécies botânicas, foram avaliados os efeitos dos extratos aquosos de Psychotria leiocarpa Cham. & Schltdl, Psychotria deflexa DC., Acosmium subelegans (Mohlenbr.) Yakovlev e Vatairea macrocarpa (Benth.) Ducke por infusão e maceração sobre os parâmetros biológicos de P. xylostella. Todos os extratos reduziram a duração larval de P. xylostella e causaram mortalidade de larvas e ovos. Nas larvas, os extratos resultaram em 70% de mortalidade. Além disso, os extratos botânicos afetaram a sobrevivência dos ovos de P. xylostella. Os extratos de P. leiocarpa e P. deflexa, preparados por infusão, retardaram a emergência dos adultos, enquanto o extrato de V. macrocarpa reduziu a sobrevivência das pupas. A longevidade dos adultos também foi influenciada pelos extratos, onde a maceração de V. macrocarpa e P. deflexa e a infusão de A. subelegans reduziram a longevidade de fêmeas de P. xylostella e a maceração de V. macrocarpa e P. leiocarpa reduziram a longevidade de machos de P. xylostella. Concluímos que os extratos estudados foram tóxicos para P. xylostella, principalmente na reprodução da traça-das-crucíferas, e consequentemente, os extratos botânicos reduziram o número de indivíduos da próxima geração.

Palavras-chave:
traça-das-crucíferas; planta inseticida; Psychotria; Acosmium subelegans; Vatairea macrocarpa

1. Introduction

The Brassicaceae family plays a significant role in the Brazilian agriculture, especially among smallscale producers (May et al., 2007; Sales, 2019). These plants hold significant commercial, nutritional, and of economic value for various regions of the country (Trani et al., 2014). According to the latest Agricultural Census, more than 187,000 Brazilian establishments were responsible for producing and distributing brassicaceous crops in 2017 (IBGE, 2022).

However, the production and commercialization of these crops face several significant challenges. Among the biotic factors, the diamondback moth Plutella xylostella L. 1758 (Plutellidae: Lepidoptera), a cosmopolitan insect, causes substantial economic losses to brassicaceous producers, significantly reducing both yield and product quality (Talekar and Shelton, 1993; Furlong et al., 2013). Moreover, the widespread application of insecticides in brassicaceous cultivation has made P. xylostella the first species reported to develop resistance to chemicals and biological agents, especially in tropical regions (Arthropod Pesticide Resistance Database, 2022). This poses a considerable challenge to farmers and results in an estimated annual cost of $4-5 billion in pest control expenses and crop losses (Zalucki et al., 2012).

In this context, there is a need for sustainable and environmentally friendly alternative methods to control P. xylostella with fewer risks to the environment and human health. While not entirely risk-free, botanical insecticides represent excellent options for pest control (Misra, 2014; Campos et al., 2019). This alternative has gained prominence due to its environmental benefits, low toxicity to mammals, and reduced risk of insect resistance (Corrêa and Salgado, 2011).

Research and using botanical insecticides align with the Sustainable Development Goals as they contribute to mitigating the impacts of climate change by reducing reliance on chemical insecticides (SDG 13 – Climate Action) and help preserve local biodiversity by preventing soil contamination and terrestrial ecosystem degradation (SDG 15 – Life on Land). Furthermore, they represent a valuable social technology that can be adopted by small-scale producers and in sustainable agricultural production (SDG 17 – Partnerships to Achieve Goals) (United Nations, 2023).

In recent years, numerous studies have been conducted to investigate botanical species' insecticidal properties and identify the most effective extraction methods for these substances. In these studies, it was found that the aqueous extract of Deguelia utilis (A.C Sm.) A.M.G Azevedo (Fabaceae) leaves reduced P. xylostella food consumption, larval survival, and oviposition in laboratory conditions. However, in field conditions, the extracts were unsuccessful (Cerda et al., 2019), while the methanol extract of leaves and bark of Stryphnodendron adstringens (Mart.) Coville (Fabaceae) at concentrations of 0.5 mg/mL, 1.0 mg/mL and 1.5 mg/mL, reduced oviposition over time for foliar samples until 96 hours of evaluation and, the hatching rate of larvae of this insect, especially at a concentration of 1.5 mg/mL (Fonseca et al., 2018). In tests involving Rubiaceae, the authors observed a reduction in the hatching rate of P. xylostella larvae that received topical applications of the aqueous extracts of Psychotria capillacea (Müll. Arg.) Standl., Psychotria carthagenensis Jacq., Psychotria deflexa DC., and Psychotria leiocarpa Cham. & Schltdl. (Silva et al., 2021a,b).

In addition to plant species and the type of extraction agent, the extraction method used to extract bioactive compounds is important. According to the literature, the solvent temperature may be favorable for extracting phenols, which are bioactive compounds with inhibitory activity against insects (Schaller, 2008; Oliveira, 2014). In the studies by Rocha et al. (2021), treatment with the aqueous extract obtained by infusion caused the lowest pupal weight, fecundity, and fertility and longevity among females.

Therefore, the objective of this study was to evaluate the effects of aqueous extracts from Psychotria leiocarpa (Rubiaceae), P. deflexa (Rubiaceae), Acosmium subelegans (Mohlenbr.) Yakovlev (Fabaceae), and Vatairea macrocarpa (Benth.) Ducke (Fabaceae) on the biological parameters of P. xylostella while comparing different extraction methods (infusion and maceration).

2. Materials and Methods

Plutella xylostella rearing, extraction preparation, and experiments were conducted in the Laboratory of Insect-Plant Interaction (LIIP) in the Infrastructure for Research on Agroenergy and Environmental Conservation (INPAC) at the Federal University of Grande Dourados (UFGD) under controlled temperature conditions of 25 ± 2 °C, a relative humidity of 60 ± 5%, and under a 12:12 (light:dark) photoperiod.

2.1. Plutella xylostella

Plutella xylostella individuals were obtained from active collections in organic gardens in the region of Dourados, Mato Grosso do Sul, and maintained in the LIIP at UFGD, following the methodology adapted from Barros et al. (2012).

The larvae were placed in plastic containers (30 cm in length × 15 cm in width × 12 cm in height). They were fed with portions of organic kale (Brassica oleracea var. acephala DC.), which had been previously sanitized with 5% sodium hypochlorite and running water. The pupae and adults of P. xylostella were kept in plastic cages measuring 9 cm in length, 19 cm in width, and 19 cm in height and were fed with a 10% honey-water solution. Organic kale discs and filter paper (8 cm in diameter) were used as substrates for oviposition. Subsequently, these discs with eggs were transferred to the caterpillar cage, starting a new development cycle (Figure 1).

Figure 1
Schematic representation of the methodology used for rearing Plutella xylostella.

2.2. Botanical material

Leaves of P. leiocarpa, P. deflexa, V. macrocarpa, and A. subelegans were collected at Mata do Azulão (Coqueiro Farm) in the municipality of Dourados (22°12'S, 54°54'W at 430 m in altitude) and at Sítio das Abelhas in the municipality of Campo Grande (21°13'28”S, 54°11'28”W at 437 m in altitude), both located in the state of Mato Grosso do Sul, Brazil. The National Research Council (CNPq)/Council for the Management of Genetic Heritage (CGEN/MMA, number 010220/2015-1) granted authorization for the collection of botanical material. One dried sample of each species was deposited in the herbarium at UFGD under the number A. subelegans (DDMS 5068), P. leiocarpa (DDMS 5007), P. deflexa (DDMS 5005), and V. macrocarpa (DDMS 5359). The collection of botanical material was authorized by the National Council for Scientific and Technological Development (Conselho Nacional de Desenvolvimento Científico e Tecnológico - CNPq) and the Council for the Management of Genetic Heritage and Associated Traditional Knowledge (SisGen) under the number A719505 (P. leiocarpa and P. deflexa), A3C7FDC (A. subelegans and V. macrocarpa).

2.3. Preparation of botanical extracts

The collected leaves were at the fourth node of the stem and totally expanded. They were washed and dried in a forced-air oven at 50 °C for three days. After drying, the material was ground in a knife mill to obtain vegetable powder. The extracts were prepared using two different extraction techniques: infusion and maceration.

The assays against P. xylostella were conducted with an aqueous extract at a concentration of 10%. To obtain the extracts by infusion, 10 g of plant powder was mixed with 100 mL of distilled water heated to approximately 80 to 85 °C. After manual stirring, the solution remained at rest for 15 minutes at room temperature (25 ± 2 °C) and was filtered with filter paper to obtain the extracts at 0.1 g/mL.

To prepare the extracts by maceration, 10 g of dried leaves were ground in a knife mill until a very fine powder was obtained. The powder was then added to 100 mL of distilled water at room temperature. After manual stirring, the solution was capped and rested for 24 hours in the refrigerator (8 °C). Then, the solution was filtered using filter paper to obtain the extracts at 0.1 g/mL.

2.4. Bioassay

Organic kale discs were cut with a metal disc measuring 4 cm in diameter, immersed for 1 minute in the treatments, and allowed to dry naturally. In Petri dishes, 5 cm in diameter, a filter paper disc moistened with distilled water, a kale disc containing the treatment, and a newly hatched caterpillar (0-24 hours) were inserted. The kale discs were replaced daily with newly treated discs until the larval stage was completed. The formed pupae were weighed on a Bel Mark Analytical Balance - 0.001 g - and stored in test tubes that were 10 cm in height and 1 cm in width until the emergence of adults, who were sexed and used in the formation of couples.

Subsequently, the pairs of P. xylostella were placed in individual cages (10 cm in diameter x 9 cm in height) containing two disks for laying eggs: one untreated kale disk on another filter paper disk (9 cm diameter). The adults were fed a 10% honey solution. Daily, the kale disks with eggs were transferred to a Petri dish, and new disks were introduced inside the cages. Petri dishes and cages were monitored daily until death.

The biological parameters evaluated were larval and pupal duration (stay in days in the stage), larval and pupal survival (percentage of individuals who reached the next stage), pupal biomass (weight of individuals in the pupal stage), fecundity (number of eggs deposited), fertility (percentage of hatched larvae), and longevity of males and females (duration of adulthood).

2.5. Statistical analysis

The experimental design was completely randomized in a 5 × 2 factorial scheme (plant x extraction method). The single factor and the interaction between the factors were evaluated using Analysis of Variance (ANOVA). Each treatment consisted of 10 replicates and 5 subsamples in the larval stage. In the adult stage, the number of possible replicates was used according to the number of live individuals in the larval stage.

The values that did not meet the assumptions were transformed, the percentage data were converted to arcsene of √x/100, and the count data were transformed to √x+0.5. After fulfilling the assumptions, the data were subjected to analysis of variance (ANOVA). When there was significance between the treatments, a means comparison test (Tukey’s test at 5% probability) was applied with the aid of R software (R Core Team, 2020).

3. Results

Regarding the interaction of the plant and extraction method factors, we observed that the biological parameters of larval duration (F = 2.03; P = 0.10; df = 4), larval survival (F = 1.38; P = 0.25; df = 4), pupal survival (F = 0.90; P = 0.44; df = 4), pupal biomass (F = 0.75; P = 0.56; df = 4), and fecundity (F = 0.77; P = 0.55; df = 4) showed no significant interactions. However, the parameters of pupal duration (F = 6.48; P = 0.0002; df = 4), fertility (F = 5.89; P = 0.0008; df = 4), and longevity of females (F = 8.12; P = 0.0007; df = 4) and males (F = 8.79; P = 0.00003; df = 4) showed interactions between the factors.

The botanical extracts prepared by maceration did not influence the pupal duration of P. xylostella; however, compared to those prepared for the control group, the extracts prepared by infusion significantly prolonged the pupal duration of P. deflexa and P. leiocarpa (Table 1).

Table 1
Pupal duration (days), egg survival (%) and adult longevity (days) of Plutella xylostella (mean ± SE) in the unfolding of the Plant x Extraction method interaction. Temperature 25 ± 1°C, Relative Humidity 60 ± 5% and under a 12:12 (light:dark) photoperiod.

Plants	Pupal duration (Days)		Egg survival (%)		Longevity of Females (Days)		Longevity of Males (Days)
	Maceration	Infusion	Maceration	Infusion	Maceration	Infusion	Maceration	Infusion
A. subelegans	5.31 ± 0.25aA n= 17	5.90 ± 0.19abA n= 12	72.3 ± 2.62bA nc= 4	58.6 ± 8.05cA nc= 4	16.0 ± 1.08aA nc= 4	10.3 ± 2.25bB nc= 4	18.3 ± 1.31aA nc= 4	15.0 ± 3.03aA nc= 4
V. macrocarpa	4.83 ± 0.20aA n= 11	5.83 ± 0.24abB n= 15	80.5 ± 3.93bA nc= 4	85.4 ± 4.92abA nc= 4	9.75 ± 0.63bB nc= 4	15.0 ± 0.41aA nc= 4	9.25 ± 1.11cB nc= 4	18.3 ± 0.73aA nc= 4
P. leiocarpa	5.50 ± 0.21aA n= 17	7.89 ± 0.52cB n= 11	73.5 ± 3.76bA nc= 7	78.2 ± 1.61bA nc= 4	11.0 ± 0.93bA nc= 7	12.5 ± 1.89abA nc= 4	12.3 ± 0.64bcB nc= 7	18.5 ± 0.29aA nc= 4
P. deflexa	5.52 ± 0.26aA n= 15	6.44 ± 0.18bB n= 15	80.6 ± 4.15bA nc= 5	52.3 ± 5.27cB nc= 4	11.0 ± 0.63bB nc= 5	15.5 ± 0.87aA nc= 4	18.0 ± 0.95aA nc= 5	16.0 ± 1.35aA nc= 4
Controle	5.46 ± 0.07aA n= 46		94.6 ± 1.08aA nc= 7		13.1 ± 0.46abA nc= 7		16.4 ± 0.87abA nc= 7
CV (%)	7.37		17.3		22.2		12.1

• Means followed by distinct letters, capital in the column and lower case in the line, differ from each other at 5% probability by Tukey's test; n= number of individuals analyzed; nc= number of couples formed.

In addition, the extracts influenced the longevity of adults, where males from the treatments with macerated V. macrocarpa and P. leiocarpa extracts presented reduced longevity when compared to those from the control. In contrast, the longevity of females increased for those treated with V. macrocarpa prepared by maceration and P. deflexa and V. macrocarpa prepared by infusion when compared to the other botanical extracts; however, this increase did not differ statistically from that in the control treatment (Table 1).

In the isolated factor plant, the parameters of pupal biomass (F = 0.86; P = 0.49; df = 4) and longevity of females (F = 1.04; P = 0.40; df = 4) and males (F = 2.24; P = 0.08; df = 4) did not show significance; however, the other biological parameters showed significance, namely, larval duration (F = 28.6; P = 0.0001; df = 4), larval survival (F = 49.6; P = 0.0001; df = 4), pupal duration (F = 5.75; P = 0.0004; df = 4), pupal survival (F = 2.65; P = 0.04; df = 4), fecundity (F = 2.61; P = 0.05; df = 4), and fertility (F = 28.8; P = 0.0001; df = 4). Additionally, all botanical species significantly reduced larval duration and caused more than 70% mortality in these individuals (Table 2).

Table 2
Larval and pupal duration (days), larval and pupal survival (%), fecundity (number of eggs) and egg survival (%) of Plutella xylostella (mean ± SE) fed with aqueous extract of Acosmium subelegans, Vatairea macrocarpa, Psychotria leiocarpa and Psychotria deflexa. Temperature 25 ± 2°C, Relative Humidity 60 ± 5% and under a 12:12 (light:dark) photoperiod.

Plants	Larval duration (days)	Larval survival (%)	Pupal duration (days)	Pupal survival (%)	Fecundity (Number of eggs)	Egg survival (%)
A. subelegans	6.48 ± 0.32a n= 100	29.0 ± 3.97b n= 100	5.64 ± 0.17b n= 29	92.6 ± 4.09ab n= 29	141.1 ± 20.7ab nc= 8	62.3 ± 4.66a nc= 8
V. macrocarpa	6.87 ± 0.44a n = 100	26.0 ± 5.25b n= 100	5.52 ± 0.22b n= 26	77.4 ± 8.31b n= 26	152.4 ± 20.4ab nc= 8	82.9 ± 3.06b nc= 8
P. leiocarpa	7.41 ± 0.44a n= 100	28.0 ± 3.95b n= 100	6.48 ± 0.38a n= 28	91.2 ± 4.78ab n= 28	139.6 ± 28.6a nc= 11	75.2 ± 2.50ab nc= 11
P. deflexa	7.74 ± 0.45a n= 100	30.0 ± 3.97b n= 100	5.93 ± 0.20ab n= 30	97.2 ± 2.78a n= 30	162.2 ± 13.0ab nc= 9	68.0 ± 5.86a nc= 9
Controle	11.8 ± 0.28b n= 100	94.0 ± 2.94a n = 100	5.46 ± 0.05b n= 94	98.0 ± 1.84a n= 94	208.4 ± 11.1b nc= 14	94.6 ± 0.73c nc= 14
CV (%)	15.0	66.1	7.37	21.7	23.7	17.3

• Means followed by different letters in the column differ from each other at 5% probability by Tukey's test; n= number of individuals analyzed; nc= number of couples formed.

In the pupal stage, the aqueous extract of P. leiocarpa delayed the emergence of adults, while the extract of V. macrocarpa reduced the survival of the P. xylostella pupae (Table 2). During the reproduction phase, the botanical extracts reduced the number of eggs, but only the extracts of P. leiocarpa caused results that were significantly different from the control. On the other hand, the botanical extracts of Fabaceae and Rubiaceae used in this experiment significantly reduced P. xylostella fertility (Table 2).

Considering the isolated factor extraction method, the parameters of larval survival (F = 0.21; P = 0.64; df = 4), pupal survival (F = 0.90; P = 0.35; df = 4), pupal biomass (F = 0.002; P = 0.96; df = 4), fecundity (F = 1.76; P = 0.19; df = 4), and longevity of females (F = 2.74; P = 0.11; df = 4) were not significant in relation to the other treatments. In contrast, the parameters larval duration (F = 4.57; P = 0.04; df = 4), pupal duration (F = 37.9; P = 0.0001; df = 4), fertility (F = 4.07; P = 0.05; df = 4), and male longevity (F = 5.82; P = 0.02; df = 4) were significant. In comparison to the extracts prepared by infusion, the extracts prepared by maceration showed higher means for larval duration and fertility. The pupal duration and longevity of males had significantly higher means in the treatments prepared by infusion than in the other treatments (Table 3).

Table 3
Larval and pupal duration (days), egg survival (%) and longevity of males (days) of Plutella xylostella (mean ± SE) fed with aqueous extract of Acosmium subelegans, Vatairea macrocarpa, Psychotria leiocarpa and Psychotria deflexa elaborated by maceration and infusion. Temperature 25 ± 2°C, Relative Humidity 60 ± 5% and under a 12:12 (light:dark) photoperiod.

Tratamento	Larval duration (days)	Pupal duration (days)	Egg survival (%)	Longevity of Males (days)
Maceration	8.40 ± 0.35a n= 250	5.40 ± 0.10a n= 134	81.1 ± 2.15a nc= 27	14.9 ± 0.74a nc= 27
Infusion	7.71 ± 0.39b n= 250	6.20 ± 0.16b n= 127	76.5 ± 3.91b nc= 23	16.8 ± 0.64b nc= 23
CV (%)	15.0	7.37	17.3	12.1

• Means followed by different letters in the column differ from each other at 5% probability by Tukey's test; n= number of individuals analyzed; nc= number of couples formed.

4. Discussion

The Rubiaceae and Fabaceae species used in this study provided satisfactory results regarding the control of P. xylostella populations because they were able to negatively affect the larval stage and the reproductive period of this insect. The larvae treated with aqueous extracts of P. leiocarpa, P. deflexa, A. subelegans, and V. macrocarpa reduced larval duration due to the early mortality of the individuals.

In previous studies, extracts from Rubiaceae and Fabaceae caused various effects on P. xylostella, such as feeding and oviposition deterrence (Egigu et al., 2010; Basukriadi and Wilkins, 2014), reduced larval hatching (Silva et al., 2021a), deformation in pupae and adults (Peres et al., 2017), reduced fecundity and adult longevity (Peres et al., 2017; Ferreira et al., 2020; Silva et al., 2020), as well as causing early mortality and reducing larval duration (Silva et al., 2020).

Bioacticity of Rubiaceae and Fabaceae was also observed in other insect groups. The saline extract of the seeds of Enterolobium contortisiliquum (Vell.) Morong (Fabaceae) caused the early death of larvae and reduced the hatching of Aedes aegypti (Linnaeus, 1762) (Diptera: Culicidae) (Barros et al., 2023). Bezerra et al. (2023) found that the essential oil of the leaves of Hymenaea courbaril L. (Fabaceae) caused the mortality of nymphs and adults of Aphis craccivora Koch (Hemiptera: Aphididae).

While the aqueous extract of the bark and leaves of Copaifera langsdorffii Desf. (Fabaceae), Coussarea hydrangeifolia (Benth.) Müll. Arg. (Rubiaceae), Guettarda angelica Mart. ex Müll. Arg. (Rubiaceae) and Rudgea viburnoides (Cham.) Benth. (Rubiaceae) caused caterpillar mortality and changes in the biological parameters of Spodoptera frugiperda (J. E. Smith, 1797) (Lepidoptera: Noctuidae) when incorporated into an artificial diet (Costa, 2015).

Souza Júnior et al. (2011), observed a 45% mortality rate in adult Sitophilus zeamais (Mots. 1855) (Coleoptera: Curculionidae) after ingestion of maize grains treated with methanolic extract of Psychotria poeppigiana Müll. Arg. (Rubiaceae) (Silva et al., 2013), while ethanol extracts of Psychotria hoffmannseggiana (Roem. & Schult.) Müll. Arg., Psychotria prunifolia (Kunth) Steyerm., and Psychotria goyazensis Müll. Arg., all belonging to Rubiaceae, showed efficiency in causing larval mortality in S. frugiperda.

A significant reduction in the survival of P. xylostella larvae after ingestion of kale treated with aqueous extract of A. intermedia and A. sessilis (Rubiaceae) (Peres et al., 2017), resulted in observations similar to those in studies with ethanolic extract of A. intermedia (Silva et al., 2020) and aqueous extract of Prosopis juliflora (Sw.) DC. (Fabaceae) (Torres et al., 2001) and with aqueous extract of D. utilis (Fabaceae) (Cerda et al., 2019).

These observations lead us to believe that individuals fed discs treated with plant extracts ingest allelochemicals that can cause early mortality, inhibit feeding after the test bite, or cause sublethal effects, such as interference in the emergence of adults, oviposition rate, viability of eggs, and population growth rate and effects on biological aspects (Seffrin et al., 2008; Carvalhinho et al., 2017). Therefore, the main sublethal effects observed in this experiment were the reduction in fecundity and the prolongation of the pupal period caused by the P. leiocarpa extracts, the reduction in the emergence of adults caused by the extracts of V. macrocarpa, the reduction in the longevity of the females caused by the extracts of P. deflexa and V. macrocarpa prepared by maceration and by the extract of A. subelegans prepared by infusion, the shortening in the longevity of males due to the extracts of V. macrocarpa and P. leiocarpa prepared by maceration, and the reduction in fertility derived from the treatments with Fabaceae and Rubiaceae extracts.

The egg reduction in the quantity and survival can be very significant in the field, as it directly affects the larvae density in the next generation and, consequently, reduces the harm and damage caused by the larvae (Maroneze and Gallegos, 2009), as well as the shortening of the period. Adults’ longevity, as they will have less time to mate and lay eggs, resulting in reduced generational growth. Some Psychotria species have larval toxicity on other Lepidoptera species. According to Tavares et al. (2013), in the ingestion test, the leaves ethanolic extracts and stems of P. hoffmannseggiana, P. prunifolia, P. goyazensis and P. capitata Ruiz & Pavon, showed efficiency greater than 80% in the mortality of S. frugiperda larvae. While the ingestion of the leaves ethanolic extract P. prunifolia caused the mortality of the larvae of Sitotroga cerealella Oliver 1819 (Lepidoptera: Gelechiidae) (Fouad et al., 2014). Leaves ethanol extracts of P. leiocarpa, Psychotria brachyceras Müll. Arg., Psychotria umbellata Ruiz & Pav. and Psychotria carthagenensis Jacq. caused larvae mortality of Helicoverpa armigera (Hübner, 1805) (Lepidoptera: Noctuidae) when fed with extracts of these plants (Matsuura et al., 2016).

Phytochemical studies have shown that Rubiaceae and Fabaceae species have tannins, quercetin, rutin, saponin and coumarin in their composition (Silva et al., 1976; Djoudi et al., 2007; Formagio et al., 2014; Formagio et al., 2019), which explains the reduction in larval survival and changes in the reproduction phase (Kaur and Rup, 2002; Cavalcante et al., 2006; Peres et al., 2017) and, in the present study the reduction in female fecundity compared to the control was observed in P. leiocarpa, while all extracts reduced egg viability.

In Rubiaceae, the presence of alkaloids is a remarkable family characteristic, with emphasis on quinolines, isoquinolines, piperidines, pyridines, indole monoterpenes (Cordell et al., 2001). In addition to these, the family also includes iridoids, flavonoids, anthraquinones, terpenoids (triterpenes and diterpenes), among others. Of these, iridoids and anthraquinones, along with indole alkaloids are considered chemotaxonomic markers for subfamilies of the Rubiaceae family (Bolzani et al., 2001).

In the genus Psychotria L. the coumarins resulting in o-coumaric acid (Czelusniak et al., 2012) and the monoterpenic indole alkaloids (Santos, 2010) are remarkable. The isolated alkaloid of P. leiocarpa is N-β-Dglycopyranosylvincosamide (Henriques et al., 2004).

The species V. macrocarpa and A. subelegans present secondary compounds with insecticidal activity in their composition, such as triterpenes, alkaloids, saponins, coumarins, flavonoids, steroids (Vieira et al., 2002; Valadares, 2017). However, there are no reports in the literature regarding the toxicity of the extract of these species on lepidopterans. We believe that the changes observed in the life cycle of P. xylostella are due to these compounds.

Under field conditions, the length of a pupal period may be relevant for producers because it increases the time of insect exposure to natural enemies and prolongs the average time of each generation, thus reducing subsequent populations and losses to producers (Torres et al., 2001). This is the first report in which the use of Rubiaceae extract prolonged the P. xylostella pupal duration. In previous studies, the authors found that the aqueous extract of A. edulis and the ethanolic extracts of A. intermedia, A. edulis, and A. sessilis did not influence the P. xylostella pupal duration, while the aqueous extracts of A. intermedia and A. sessilis delayed adult emergence (Kaur and Rup, 2002; Silva et al., 2020).

Phytochemical studies have shown that Rubiaceae and Fabaceae species contain tannins, quercetin, rutin, saponin, and coumarin (Djoudi et al., 2007; Formagio et al., 2014), which explains the reduction in larval survival and changes in the reproduction phase (Kaur and Rup, 2002; Cavalcante et al., 2006; Peres et al., 2017). In the present study, it was found that in comparison to the control, the aqueous extract of P. leiocarpa reduced female fecundity, while all extracts reduced egg viability.

A similar effect when using an aqueous extract of A. intermedia on P. xylostella was linked to the presence of rutin in the chemical composition of the plant (Peres et al., 2017). On the other hand, compared to the control, the ethanolic extract of A. intermedia increased the fecundity of P. xylostella and reduced its fertility (Silva et al., 2020). After treatment with aqueous extracts of P. juliflora and Leucaena leucocephala (Lam) De Wit (Fabaceae), fecundity and fertility of Bemisia tabaci (Gennadius 1889) (Hemiptera: Aleyrodidae) were significantly reduced, while the aqueous extract of Mimosa caesalpiniifolia Benth (Fabaceae) altered only the fecundity of this insect (Cavalcante et al., 2006).

Reductions in quantity and fertility can be very significant in the field, as they directly affect the density of larvae in the next generation and consequently reduce damage caused by larvae (Maroneze and Gallegos, 2009), as well as the shorten adult longevity, because they have less time to mate and lay eggs, resulting in reduced generation growth.

The results also showed that the extracts prepared by maceration and infusion had generally the same effect on the insect. The efficacy of an extract is influenced by various factors, such as the solvent type (methanol, ethanol, water, or hexane), plant species, plant part used (root, stem, leaf, fruit, or flower), and species of the target insect, as well as the type of extraction (maceration, infusion, or decoction) and the solvent temperature (Fonsêca, 2005; Oliveira, 2014).

5. Conclusions

We conclude that the aqueous extracts of P. leiocarpa, P. deflexa, A. subelegans and V. macrocarpa, regardless of the extraction method are toxic to the biological parameters of P. xylostella, especially the parameters that affect future generations. We emphasize that the results were obtained under controlled laboratory conditions. Therefore, in addition to determining the bioactive compounds present in the extracts, it is also necessary to perform semifield and field tests to better understand the mode of action of the botanical species. We reiterate that it is essential to conduct studies to verify the toxicity of these extracts in non-target organisms, to ensure that their use does not inadvertently harm the environment.

Research with botanical extracts demonstrates the possibility of developing more sustainable alternatives in agricultural pest control, reducing reliance on chemical pesticides. This approach aligns with sustainable development, promoting environmental preservation, food security, and biodiversity protection while also seeking effective solutions to the challenges of modern agriculture.

Acknowledgements

We thank the Laboratory of Insect-Plant Interaction at the Federal University of Grande Dourados for logistical support; the National Council for the Improvement of Higher Education-Brazil (CAPES) for the scholarship for the first author, and the Foundation for Support to the Development of Teaching, Science and Technology of the State of Mato Grosso do Sul (FUNDECT) for the resource provided by grant no. 83/029.649/2024; We would like to thank CNPq for the Research Productivity grant (Rosilda Mara Mussury) and the Technological Development and Innovative Extension Productivity grant (Juliana Rosa Carrijo Mauad); and Dr. Zefa Valdivina Pereira for the identification of the botanical species.

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Publication Dates

• Publication in this collection
  14 Mar 2025
• Date of issue
  2024

History

• Received
  03 Feb 2024
• Accepted
  01 Aug 2024
• Corrected
  14 Mar 2025