Selectivity of water-based extracts of Serjania spp. on Tetrastichus howardi (Hymenoptera: Eulophidae), an endoparasitoid of Plutella xylostella (Lepidoptera: Plutellidae)Abstract
The use of botanical insecticides is a sustainable alternative for the regulation of Plutella xylostella (Linnaeus, 1758) (Lepidoptera: Plutellidae) in brassica crops. Similarly, biological control with parasitoids can be an effective tool when integrated with bioinsecticides. However, the safety of natural insect enemies must be prioritized within pest control programs. The objective was to evaluate the effects of the water-based extracts of Serjania erecta Radlk (Sapindaceae) and Serjania marginata Casar (Sapindaceae), at 5% and 10% concentrations, on the reproduction of Tetrastichus howardi (Olliff, 1893) (Hymenoptera: Eulophidae) in larvae of P. xylostella, topically treated with extracts. In addition, we evaluated the survival of adult females of T. howardi exposed to the respective extracts of Serjania spp. For this purpose, two bioassays were conducted. In the first, 4th instar larvae of P. xylostella were selected, and 20 μL of each treatment was applied topically (S. erecta 5%, S. erecta 10%, S. marginata 5%, S. marginata 10%, distilled water) in each larva and then exposed to T. howardi parasitism for 48 hours. The percentage of parasitism and emergence (%), life cycle length (days), total number of progeny, sex ratio and adult longevity were evaluated. In the second bioassay, the ASPECLE (Evaluation of Pesticide Selectivity under Extended Laboratory Conditions) system, adapted from the International Organization for Biological Control (IOBC) standard model, was used. In this bioassay, five cabbage leaf disks were introduced in each glass cylinder of the ASPECLE system, duly treated with distilled water, aqueous extracts of S. erecta and S. marginata, at concentrations of 5% and 10%, or acephate. Subsequently, ten adult females of T. howardi were released in each cylinder and the system was activated. Parasitoid survival was evaluated for 24, 48, 72, 96 and 120 hours. The aqueous extracts of S. marginata and S. erecta at concentrations of 5% and 10% did not interfere in the parasitism of T. howardi on 4th instar larvae of P. xylostella. Field experiments should be developed to prove the negative effect of aqueous extracts of S. marginata and S. erecta on other biological characteristics of T. howardi. As a precaution, releases of T. howardi and sprays of aqueous extracts of S. marginata and S. erecta should be made at different times for the biological management of P. xylostella.
Keywords:
bioinsecticides; Serjania erecta; Serjania marginata; parasitoid; selectivity
Resumo
O uso de inseticidas botânicos é uma alternativa sustentável para a regulação de Plutella xylostella (Linnaeus, 1758) (Lepidoptera: Plutellidae) em culturas de brássicas. Da mesma forma, o controle biológico com parasitóides pode ser uma ferramenta eficaz quando integrado a bioinseticidas. No entanto, a segurança dos inimigos naturais dos insetos deve ser priorizada nos programas de controlo de pragas. Objetivou-se avaliar os efeitos dos extratos aquosos de Serjania erecta Radlk (Sapindaceae) e Serjania marginata Casar (Sapindaceae), nas concentrações de 5% e 10%, na reprodução de Tetrastichus howardi (Olliff, 1893) (Hymenoptera: Eulophidae) em larvas de P. xylostella, tratadas topicamente com extratos. Além disso, avaliamos a sobrevivência de fêmeas adultas de T. howardi expostas aos respectivos extratos de Serjania spp.. Para tanto, foram realizados dois bioensaios. No primeiro foram selecionadas larvas de 4º ínstar de P. xylostella e aplicados topicamente 20 μL de cada tratamento (S. erecta 5%, S. erecta 10%, S. marginata 5%, S. marginata 10%, água destilada) em cada larva e depois exposta ao parasitismo de T. howardi por 48 horas. Foram avaliadas a porcentagem de parasitismo e emergência (%), duração do ciclo de vida (dias), número total de progênies, razão sexual e longevidade dos adultos. No segundo bioensaio, foi utilizado o sistema ASPECLE (Avaliação da Seletividade de Pesticidas Sob Condições Laboratoriais Estendidas), adaptado do modelo padrão da Organização Internacional para Controle Biológico (IOBC). Neste bioensaio foram introduzidos cinco discos de folhas de repolho em cada cilindro de vidro do sistema ASPECLE, devidamente tratados com água destilada, extratos aquosos de S. erecta e S. marginata, nas concentrações de 5% e 10%, ou acefato. Posteriormente, dez fêmeas adultas de T. howardi foram liberadas em cada cilindro e o sistema foi acionado. A sobrevivência dos parasitóides foi avaliada por 24, 48, 72, 96 e 120 horas. Os extratos aquosos de S. marginata e S. erecta nas concentrações de 5% e 10% não interferiram no parasitismo de T. howardi sobre larvas de 4º ínstar de P. xylostella. Experimentos de campo deverão ser desenvolvidos para comprovar o efeito negativo dos extratos aquosos de S. marginata e S. erecta sobre outras características biológicas de T. howardi. Por precaução, liberações de T. howardi e pulverizações de extratos aquosos de S. marginata e S. erecta devem ser feitas em momentos diferentes para o manejo biológico de P. xylostella.
Palavras-chave:
bioinseticidas; Serjania erecta; Serjania marginata; parasitoides; seletividade
1. Introduction
Parasitoids are responsible for balancing the population density of several phytophagous insects in several agricultural production systems (Dolphin and Quicke, 2001; Stiling and Cornelissen, 2005; Kaur et al., 2021), as an example the parasitoid Tetrastichus howardi (Olliff, 1893) (Hymenoptera: Eulophidae) that has been reported in some studies parasitizing different hosts (Cruz et al., 2011; Favoreto et al., 2021; Rodrigues et al., 2021), including Plutella xylostella (Linnaeus, 1758) (Lepidoptera: Plutellidae), being an important natural enemy of this insect (Silva-Torres et al., 2010).
Biological control can be an effective tool when associated with other control techniques offered by Integrated Pest Management (MIP), such as the use of botanical insecticides (Monsreal-Ceballos et al., 2018). The use of bioinsecticides, as well as parasitoids employed in biological control, is an alternative and environmentally sound control method, given the presence of allelochemicals present in plant metabolites that act against herbivory (flavonoids, alkaloids, terpenoids, saponins, and phytohormones) (Isman, 2006).
Some studies have already been developed to investigate the insecticidal activity of plant species against certain pests of economic importance in agriculture (Sajjad et al., 2017; Fite et al., 2018; Majeed et al., 2018; Rioba and Stevenson, 2020), including for P. xylostella (Peres et al., 2017; Couto et al., 2019, 2020; Ferreira et al., 2020; Faca et al., 2021; Rocha et al., 2022; Padial et al., 2023). Several botanical families such as Meliaceae, Onagraceae, Asteraceae, Rutaceae, Euphorbiaceae, Solanaceae, Annonaceae, Anacardiaceae, Rubiaceae, Commelinaceae, Melastomataceae and Sapindaceae have already been investigated aiming to determine their activities on the biological characteristics of insects, for future development of bioinsecticides (Jacobson, 1989; Amoabeng et al., 2013; Krinski and Massaroliet al., 2014; Peres et al., 2017; Couto et al., 2020; Ferreira et al., 2020). The Sapindaceae family presents several genera and species with potential insecticidal action, such as the genus Serjania that has already been reported for the control of P. xylostella (Couto et al., 2019, 2020; Faca et al., 2021).
Plutella xylostella is one of the main pests of economic interest in the brassica crop, being responsible for significant damage to this crop (Li et al., 2016). The main method currently employed for the control of P. xylostella is the chemical one, because it ensures immediate reduction of high populations of this insect, however, successive applications of pesticides can contribute to the increase of the selection pressure of these insects, contributing to the emergence of resistant populations and making the control even more complex (Yu et al., 2015; Arruda et al., 2020).
Several authors report the concern and importance of raising awareness about the use of chemicals and their reach on non-target organisms, by developing work on insecticide selectivity on beneficial organisms (Kumar et al., 2018; Jiang et al., 2019; Lu et al., 2020; Ricupero et al., 2020; Sanomia et al., 2020; Gonçalves et al., 2021), including on the natural enemies of P. xylostella (Bacci et al., 2018; Rahardjo et al., 2021). Given the need to contain the high populations of P. xylostella in vegetable crops, using alternative and interactive methods for its control, and in view of the importance of preserving its natural enemies, the aim of this research was to evaluate the selectivity of aqueous extracts of Serjania erecta Radlk. (Sapindaceae) and Serjania marginata Casar. (Sapindaceae) at concentrations 5% and 10%, on the reproduction and adults of T. howardi.
2. Materials and Methods
The extracts and bioassays were prepared and performed at the Laboratory of Insect–Plant Interaction (LIIP) and Laboratory of Biological Control of Insects (LECOBIOL), School of Biological and Environmental Sciences, Federal University of Grande Dourados (UFGD), Dourados, Mato Grosso do Sul, Brazil.
2.1. Rearing of P. xylostella
To establish P. xylostella rearing, pupae and larvae were collected from Brassica oleracea var. acephala (Brassicaceae) cultivation areas in the municipality of Dourados, Mato Grosso do Sul, Brazil (22°15'59.7”S 54°48'31.9”W). Subsequently, the rearing was maintained and multiplied under controlled conditions of temperature (25 ± 2 °C), relative humidity (RH) (55 ± 5%) and 12-h photoperiod at the Laboratory of Insect-Plant Interaction of the Federal University of Grande Dourados (LIIP-UFGD), Mato Grosso do Sul, Brazil (22°11'56.9”S 54°56'00.4”W).
The pupae were placed in clear plastic cages (9 cm long × 19 cm wide × 19 cm high) until adult emergence. The adults were fed 10% honey and kale disks (8 cm in diameter) on filter paper for oviposition by females. The kale leaf discs containing the egg masses were replaced daily and transferred to properly sterilized and sanitized clear plastic pots (30 cm long × 15 cm wide × 12 cm high). The newly hatched larvae were fed organic kale (Brassica oleracea var. acephala) leaves that were properly sanitized and washed with 5% sodium hypochlorite solution and running water. The kale leaves were placed in pots with the adaxial side facing the plastic container and the abaxial side facing up, to which the larvae were introduced. Next, another kale leaf was placed with the abaxial side facing the larvae. The leaves were replaced daily, always keeping the upper leaves, and the larvae remained in the pots until they reached the pupal stage (Barros et al., 2012).
2.2. Identification and rearing of the parasitoid T. howardi
The parasitoid used in this study was collected from pupae of Diatraea saccharalis (Fabricius, 1794) (Lepidoptera: Crambidae) at the Agricultural Sciences Experimental Farm (FAECA) of Federal University of Grande Dourados (UFGD) (22° 13' 16” S, 54° 48' 2” W, 530 m.a.s.l.) inside sugarcane stalks in December 2010. The specimens were deposited in the Entomological Collection of the Department of Biological Sciences of Federal University of Espírito Santo (UFES) under accession number 150792 to 150816 and 157187 (data available online at Splink).
The adult parasitoids of T. howardi were reared in glass tubes measuring 15 × 2 cm and covered with cotton and fed a droplet of honey. Pupae of D. saccharalis aged 24 to 48 hours were exposed to parasitism by five females of T. howardi for 24 hours in an air-conditioned chamber under controlled conditions (temperature 25 ± 2 °C, RH of 70 ± 10% and 14-hour photoperiod). After approximately 20 days, the parasitoids emerged and were properly fed a droplet of honey and allowed to mate for 24 hours. After this period, the insects were sexed, and the females were individually placed in glass tubes to conduct the bioassays (Vargas et al., 2011).
2.3. Botanical material
Expanded leaves of S. erecta and S. marginata were collected at the Medicinal Plant Garden (HPM) of the Federal University of Grande Dourados, in Dourados, Mato Grosso do Sul, Brazil (22°11’43.7” S and 54°56’08.5” W).
The species were identified from the exsiccata present in the herbarium of the Federal University of Grande Dourados, with the respective registration numbers: 5395 (S. erecta) and 6267 (S. marginata).
2.4. Preparation of aqueous extracts
The expanded leaves collected from S. erecta and S. marginata were placed in a forced air circulation chamber for three days at a constant temperature of 40 °C (±1 °C). Subsequently, the leaves were ground using an industrial knife mill until a fine powder was obtained.
The aqueous extracts were prepared using the maceration technique, where 5 g and 10 g of the plant material were mixed with 50 mL of distilled water to obtain concentrations of 10% and 5%, respectively. After manual agitation, the extracts were cooled to 10 °C for 24 hours for the extraction of water-soluble compounds. Next, the solution was strained through voile fabric to obtain the extracts at concentrations (weight/volume) of 5% and 10%.
2.5. Experimental procedures
2.5.1. Bioassay 1: reproduction of T. howardi on P. xylostella larvae topically treated with aqueous extracts of Serjania spp.
The experimental procedure was adapted from the methodology of Rampelotti-Ferreira et al. (2017) and Bersani et al. (2020). Fourth-instar larvae of P. xylostella were selected from the LIIP-UFGD. The larvae were individually placed in Petri dishes lined with filter paper, and 20 μL of each treatment (distilled water, 5% S. erecta extract, 10% S. erecta extract, 5% S. marginata extract or 10% S. marginata extract) was placed directly on the dorsal surface of each larva with the aid of a digital micropipette. After drying naturally, the larvae were individually placed in glass tubes (15 × 2 cm) female T. howardi aged 24 hours that had already mated and fed. The tubes were covered with cotton, a droplet of honey was inserted to feed the parasitoid and a piece of kale leaf was inserted to feed the fourth-instar larvae until they reached the pupal stage. Parasitism was allowed to occur for 48 hours, and after this period, the females of T. howardi were removed, and the tubes containing the parasitized hosts were placed in a BOD incubator under controlled temperature, RH and photoperiod of 25 °C, 70% and 12 hours until adult emergence (Figure 1).
Schematic representation of the experiment conducted for T. howardi reproduction on fourth-instar larvae of P. xylostella treated topically with aqueous extracts of Serjania spp. at 5% and 10% concentrations (temperature 25 ± 2 °C, RH 70 ± 10% and 14-hour photoperiod).
The following biological traits were evaluated: percentage of parasitism (%) and emergence (%), life cycle duration (days), total number of progeny, number of female progeny, number of male progeny, sex ratio, and male and female longevity. The symptomatological characteristics of P. xylostella larvae and pupae under parasitism by T. howardi were a mummified appearance, brown and black coloration, and a dry, stiff brown tegument.
2.5.2. Bioassay 2: Survival of T. howardi females exposed to aqueous extracts of Serjania spp.
The ASPECLE system (Assessment of Pesticide Selectivity under Extended Laboratory Conditions) adapted from the International Organization for Biological Control (IOBC) standard model was used. In this study, the system was adapted from Sanomia et al. (2020) for the evaluation of the selectivity of botanical aqueous extracts and their biological safety in adults of T. howardi.
The ASPECLE system consisted of a ventilation system based on an aspirator/compressor with a vacuum pump (Model 089/Cal, Fanem™, São Paulo, SP, Brazil), which was responsible for aspirating the toxic gases from the cage. The pump was connected directly to a 2.20-cm-diameter central tube (random polypropylene copolymer - RPP, Amanco™, São Paulo, SP, Brazil) by a 1.00-cm-diameter × 100-cm-long hose. The central tube distributed the suction of the vacuum pump among all the cages through several hoses measuring 0.50 cm in diameter × 13.00 cm in length.
The black plastic and circular voile fabric placed together with the caps at the ends of the tubes were used to seal the tubes and prevent the parasitoids from going to the ends of the tubes. Cylinders made of green cardboard (3.60 cm diameter × 8.00 cm long) were superimposed on the tubes to produce shade and encourage the parasitoids to remain in the center of the cage on the treated substrate.
The treatments used in this experiment were distilled water (negative control), aqueous extracts of S. erecta and S. marginata at 5% and 10% concentrations, and acephate (positive control). Kale leaf discs measuring 8 cm in diameter were immersed in the respective treatments and left to dry. Next, five kale leaf discs immersed in the same treatment were introduced into the glass cages. The cages were properly capped and connected by hoses to the central tube. Ten properly fed adult T. howardi females were released into each cage, and the vacuum pump was turned on, activating the ASPECLE ventilation system. The ventilation system was turned off, and the cages were disconnected after 120 hours of experimental evaluation.
The bioassay was performed in an acclimatized room with a temperature of 25 ± 2 °C, relative humidity of 70 ± 10% and 14-hour photoperiod. The survival of T. howardi females at 24, 48, 72, 96 and 120 hours of exposure to the respective treatments was evaluated.
2.6. Statistical analysis
The experiment for bioassay 1 was performed using a completely randomized design with two factors (3×2), consisting of two plant species, one control and two aqueous extract concentrations, with 10 replicates of 5 subsamples, totaling 50 fourth-instar larvae per treatment. The data were checked for normality using the Shapiro‒Wilk test and, when necessary, √x + 0.5 and arcsine √x/100 transformed. The results were subjected to analysis of variance, and the means were compared using Tukey’s test (p < 0.05). Data were analyzed on the R platform.
Bioassay 2 consisted of 12 replicates of 10 subsamples, totaling 120 parasitoids per treatment. The survival curves of T. howardi were estimated using the Kaplan‒Meier method and compared between treatments (insecticides and control) for each product tested by the log-rank test using the LIFETEST procedure of SAS (SAS Institute, 2001).
3. Results
3.1. Bioassay 01: Reproduction of T. howardi on P. xylostella larvae topically treated with aqueous extracts of Serjania spp.
There was a significant interaction between plant and concentration factors only for sex ratio (F =3.9131; DG = 2; p = 0.0258815) (Table 1). Serjania erecta at the 5% concentration was responsible for the lowest sex ratio evaluated. While S. marginata at 5% and 10% concentration did not influence the sex ratio of T. howardi progeny equaling the control (Table 1).
Interaction between plant and concentration for sex ratio of Tetrastichus howardi reproduced in the host Plutella xylostella treated topically with aqueous extracts of Serjania erecta and Serjania marginata at concentrations 5% and 10%.
There was significance for the single plant factor for the percentage of emergence (F = 10.9809; DF = 2; p = 0.00010), male progeny number (F = 12.3661; DF = 2; p = 0.000038) and male longevity (F = 3.2389; GL = 2; p = 0.049186) (Table 2). There was significance for the single concentration factor only for male longevity (F = 4.7767; DF = 1; p = 0.034476).
Biological characteristics of Tetrastichus howardi reproduced in 4th instar larvae of Plutella xylostella treated topically with aqueous extracts of Serjania spp. (temperature 25 ± 2 °C, relative humidity (RH) 70 ± 10% and 14 hr photophase).
The plant extracts did not influence the percentage of parasitism of T. howardi, showing parasitism rate above 87.00% in all treatments, however, both species caused a reduction in the percentage of progeny emergence, presenting a minimum percentage of 58.00% (Table 2). The aqueous extracts of S. erecta and S. marginata also did not influence the number of female progeny or their longevity, however, the extracts of S. erecta induced an increase in the number of male progeny (Table 2). Male longevity decreased in the treatment containing aqueous extracts of S. marginata. Moreover, the 5% concentration in the isolated factor concentration was responsible for the decrease in longevity (Table 2).
According to the standards established by IOBC, the results suggest that Serjania spp. extracts belong to Class I of toxicity, being classified as innocuous (<30%), characterized by low mortality of T. howardi.
3.2. Survival of T. howardi females exposed to aqueous extracts of Serjania spp.
The survival of the parasitoid T. howardi was influenced by the different treatments tested (χ2 = 714.87; DF = 5; p <0.0001) (Figure 2). Thus, the mean time the parasitoid survived in hours was shorter than the mean ± SE de 114.15 ± 1.32, 111.73 ± 1.51, 115.72 ± 1.03, 109.4 ± 1.84, 112.13 ± 1.55 and 24 ± 0.00 for testimony, S. erecta 5%, S. erecta 10%, S. marginata 5%, S. marginata 10% and acephate, respectively. That is, the aqueous extracts of Serjania spp. were less selective and did not show shock effect as demonstrated by acephate for females of the parasitoid T. howardi, reducing survival of T. howardi statistically similar to the control (distilled water), however, the treatment containing acephate (positive control) was statistically different, as there was no survival in this treatment.
Survival curve of T. howardi females exposed to aqueous extracts of Serjania spp. for 24, 48, 72, 96 and 120 hours under controlled laboratory conditions (temperature 25 ± 2 ºC, relative humidity 70 ± 10% and 14 h photoperiod).
4. Discussion
Pesticide applications in the field for the control of agricultural pests can compromise the local beneficial entomofauna, especially natural enemies that can be directly affected by direct contact with insecticides, either during the foraging process or during their feeding (Nidagundi et al., 2021). The interaction of pest control methods involving pesticides and biological control should prioritize the preservation of biodiversity and the local ecosystem, and tests are needed to ensure the safety of the environment and non-target organisms (Carvalho et al., 2019; Pisa et al., 2021).
Some parasitoids are constantly affected by pesticides and studies reveal that certain products can be highly toxic, harmful and persistent to these insects (Cheng et al., 2018, 2021; Khan, 2020). In addition to pesticides, bioinsecticides, despite presenting a number of advantages from their practicality to their low persistence, are also constantly being investigated for their negative effects on parasitoids, as they can compromise the biology of these agents, affecting parasitism, emergence and their survival (Tunca et al., 2012, 2014; Monsreal-Ceballos et al., 2018). Little is known regarding the effects of aqueous extracts of the plant species S. erecta and S. marginata on the biology, reproduction, and survival of T. howardi.
According to the results obtained, the percentage of parasitism of T. howardi was not affected by the aqueous extracts of S. erecta and S. marginata and in any of the concentrations evaluated. Allelochemicals, present in botanical extracts, can attract the parasitoids to the host, facilitating localization and parasitism (Charleston et al., 2006; Liu et al., 2006). Because of this, some botanical extracts can stimulate the increase of parasitism percentage (Charleston et al., 205) through chemical substances, coming from the secondary metabolite of plants, such as alkaloids, flavonoids, terpenes and phenolic compounds (Bruce and Cork, 2001; Senthil-Nathan et al., 2008). Thus, the botanical extracts did not interfere with the percentage of parasitism, since secondary metabolites can be attractive to natural enemies, since phytochemical analyses of S. erecta and S. marginata prove the presence of phenolic compounds, flavonoids, tannins and saponins in the composition of these plant species (Gomig et al., 2008; Moreira et al., 2019).
The percentage of emergence decreased in treatments that used the aqueous extracts of S. erecta and S. marginata, possibly due to the influence of secondary metabolites present in the treatments. Some bioinsecticides can interfere with the parasitoid larval ecdysis process, partially or completely inhibiting its larval growth inside the host, preventing the development and emergence of adult individuals (Beckage et al., 1998). Tunca et al. (2014), observed the reduction in the percentage of emergence of the parasitoid Chelonus oculator (Panzer, 1806) (Hymenoptera: Braconidae) exposed to botanical insecticides based on azadirachtin and pyrethrum. Boeke et al. (2003) also observed the low emergence percentage of the egg parasitoid Uscana lariophaga (Steffan, 1954) (Hymenoptera: Trichogrammatidae) from treatment containing Nicotiana tabacum L. (Solanaceae). Like S. erecta and S. marginata, N. tabacum also presents in its composition phenolic compounds, flavonoids and polyphenols and these compounds have already been reported presenting insecticidal action (Sarwar, 2015; Zou et al., 2021). Perera et al. (2000) observed a significant reduction in the percentage of emergence of the parasitoid and Cotesia plutellae (Kurdjumov, 1912) (Hymenoptera: Braconidae) on P. xylostella in treatments with vegetable oil.
The life cycle of T. howardi did not show significant differences between treatments (control or aqueous extracts of Serjania spp.), however, the development cycle of T. howardi can vary according to the host chosen, being reported approximately, 15 days for pupae of Helicoverpa armigera (Hübner, 1805) (Lepidoptera: Noctuidae) and 16 days for pupae of Oxydia vesulia (Cramer, 1779) (Lepidoptera: Geometridae) (Oliveira et al., 2016; Favoreto et al., 2021).
The sex ratio was lower for the 5% S. erecta treatment, showing a higher number of males in this treatment. Campos-Farinha et al. (2000) suggest that when the parasitoid does not find a suitable host for the development of its offspring, there is a reduction in sex ratio, expressed by an increase in the number of male progeny, which when they become adults will copulate with more females, increasing the percentage of parasitism and progeny. Furthermore, the quality, size and nutritional resources of the host are directly related to the process of choice, parasitism and development of the parasitoid (Godfray, 1994). Charleston et al. (2005) observed from sex ratio a biased increase in male development of C. plutellae in P. xylostella larvae treated with botanical extracts.
The longevity of females did not change significantly between treatments, showing that S. erecta and S. marginata did not influence this characteristic. Male longevity decreased for S. marginata, surviving approximately 14 days, but was higher in the 10% concentration, surviving approximately 18 days. Tunca et al. (2014) also noted reduced longevity of males and females in treatments containing doses of botanical insecticides.
The survival of adult females of T. howardi was not affected by the different extracts of Serjania spp. and concentrations (5% and 10%), being able to integrate the biological control method, together with applications of bioinsecticides from the studied plants. Some authors reveal the safety of certain botanical insecticides for some parasitoid insects and highlight the importance of the interaction of these two tools for the successful control of insect populations within an integrated pest management program (Hassan et al., 2022). Novio et al. (2020) studied the effect of extracts produced from seeds of Annona squamosa L. (Annonaceae) and Mangifera altissima Blanco (Anacardiaceae), rich in phenols, saponins and tannins, and found that they were toxic to the pest, however, less potent for the endoparasitoid Tetrastichus brontispae (Ferrière, 1933) (Hymenoptera: Eulophidae), and can be integrated into biological control programs.
Field experiments should be developed to prove the negative effect of aqueous extracts of S. marginata and S. erecta on the other biological characteristics of T. howardi. As a precaution, releases of T. howardi and sprays of aqueous extracts of S. marginata and S. erecta should be performed at different times for the biological management of P. xylostella.
5. Conclusions
The water-based extracts of S. marginata and S. erecta, at concentrations of 5% and 10%, did not interfere in the parasitism of T. howardi on 4th instar larvae of P. xylostella. In general, water-based extracts of S. marginata and S. erecta, at concentrations of 5% and 10%, negatively interfered on the emergence, sex ratio and longevity of T. howardi males on 4th instar larvae of P. xylostella.
Acknowledgements
We thank the Laboratory of Insect-Plant Interaction and Laboratory of Biological Control of Insects, 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; and Dr. Zefa Valdivina Pereira for the identification of the botanical specie. We thank the CNPq for the Research Productivity grant (Rosilda Mara Mussury and Fabricio Fagundes Pereira) and financial support to Itaipu Binacional and Itaipu Parquetec.
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