Investigating the selectivity of botanical and synthetic insecticides on Doru luteipes: there is no simple answer

Investigating the selectivity of botanical and synthetic insecticides on Doru luteipes: there is no simple answer | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Research Article Investigating the selectivity of botanical and synthetic insecticides on Doru luteipes: there is no simple answer Emile Dayara Rabelo Santana, Leonardo Vinicius Thiesen, Mariana Yamada, and 4 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-5823057/v1 This work is licensed under a CC BY 4.0 License Status: Under Review Version 1 posted 4 You are reading this latest preprint version Abstract To achieve sustainability in agricultural pest management, it is essential to integrate chemical and biological control through selectivity studies. In this study, we evaluated the lethal and sublethal effects of both botanical and synthetic insecticides used for controlling the fall armyworm, Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae), on its natural enemy Doru luteipes (Scudder) (Dermaptera: Forficulidae). For this purpose, bioassays of mortality, behavior, and transgenerational effects were conducted. Botanical insecticides rich in acetogenins and limonoids caused less than 30% mortality in D. luteipes nymphs (2nd, 3rd, and 4th instars). In contrast, chlorantraniliprole-based insecticide (Premio®) was highly toxic, presenting mortality above 80% at all nymphal stages and reducing predation capacity by 55.97% and walking velocity by 28.44% compared to the control. Aqueous emulsion of the ethanolic extract from Annona mucosa seeds (ESAM) reduced the longevity of the adults to 88.88 days. Chlorantraniliprole resulted in the shortest pre-oviposition period (9.44 days), followed by a limonoids-based botanical insecticide (Azamax®) (11.00 days). Fourth-instar nymphs of the F 1 generation showed lower viability (54.54%) in the treatment with aqueous emulsion of the methanolic fraction from Annona montana leaves (EFAMON). The annonin-based commercial botanical insecticide (Anosom®) affected life table parameters, reducing the intrinsic growth rate ( r m = 0.039) and finite rate of increase ( λ = 1.04). These findings indicate that botanical insecticides are less hazardous to the natural enemy D. luteipes than synthetic insecticide. This study provides important insights for improving pest control while preserving natural enemies. Non-target organisms Acetogenins Limonoids Biological control Sublethal effects Figures Figure 1 Figure 2 Figure 3 Figure 4 Introduction Combining chemical and biological control is a key precept in Integrated Pest Management (IPM) programs, and selectivity studies provide essential information for this achievement. In this context, a selective compound should effectively control the target pest while minimizing adverse effects on natural enemies (Castle and Naranjo 2009 ; Gentz et al. 2010 ; Bueno et al. 2017 ; Torres and Bueno 2018 ; Serrão et al. 2022 ). Recent efforts have focused on ensuring that newly introduced insecticide molecules are environmentally friendly, promoting a better agroecosystem balance. Examples of these new molecules include botanical insecticides, considered promising alternatives for pest management and less harmful to non-target organisms, along with organosynthetic compounds such as diamides (Ishaaya et al. 2007 ; Turchen et al. 2014 ; Gontijo et al. 2015 ; Ndakidemi et al. 2016 ; Bernardi et al. 2017 ; Rezende-Teixeira et al. 2022 ; Sparks and Bryant 2022 ; Cong et al. 2023 ; Schmidt-Jeffris 2023 ). The fall armyworm, Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae), is a significant agricultural pest that affects economically important crops, such as corn, cotton, soybean, rice, and wheat. Control efforts have been challenged by resistance to various chemical groups and Bt corn, which has intensified the search for new management alternatives (Montezano et al. 2018 ; Tay et al. 2023 ; Mota-Sanchez and Wise 2024 ). Among the promising options are botanical insecticides, such as extracts from Annona mucosa and Annona montana plants, and the commercial botanical insecticide Anosom®, derived from Annona squamosa plant. These compounds are rich in acetogenins, a class of natural products consisting of long-chain fatty acids with a 2-propanol unit, and they exhibit distinct modes of action (Colom et al. 2009 ; Di Toto Blessing et al. 2012 ; Ansante et al. 2015 , 2017 ; Costa et al. 2016 ; Hidalgoa et al. 2020 ). Other registered compounds for controlling S. frugiperda include the commercial botanical insecticide Azamax®, which is based on azadirachtin and 3-tigloylazadiractol from the Azadirachta indica plant, and the commercial organosynthetic insecticide Premio®, whose active ingredient is chlorantraniliprole, belonging to the diamide group (MAPA, 2024 ). Effective management of S. frugiperda requires that the use of chemical insecticides be compatible with the natural enemies involved in biological control, such as the predator Doru luteipes (Scudder) (Dermaptera: Forficulidae). This predator is commonly found in corn crops, feeding on eggs and larvae of S. frugiperda . Nymphs of D. luteipes can consume up to 10 eggs or larvae per day, while adults can consume up to 20 first- and second-instar larvae (Cruz et al. 1995 ; Cruz 2007 ; Pasini et al. 2010 ; Pacheco 2019 ). Additionally, as a polyphagous predator, D. luteipes is capable of preying on other agriculturally significant pests (Romero Sueldo and Virila 2009 ; Romero Sueldo et al. 2014 ; Silva et al. 2023 ). However, achieving compatibility between chemical insecticides and natural enemies can be challenging. Selectivity depends on several factors, including the product's physicochemical composition, the target species, the method of exposure, the insect's developmental stages, its behavior, and its detoxification mechanisms (Godoy et al. 2010 ; He et al. 2019 ; Vázquez 2019 ; Silva et al. 2020 ; Potin et al. 2022 ). Although most of the insecticides mentioned earlier for controlling S. frugiperda are derived from botanical sources, and the organosynthetic insecticide (chlorantraniliprole) is reported to be selective towards non-target organisms, ecotoxicology studies need to be conducted considering the specific characteristics of the pest, the insecticide, the natural enemy, and the exposure method (Gontijo et al. 2015 ; Haddi et al. 2020 ; Serrão et al. 2022 ; Arroyo et al. 2023 ). Moreover, these studies should assess not only direct lethal effects but also sublethal effects, which may compromise the effectiveness of natural enemies and the sustainability of agricultural system (Haddi et al. 2020 ).(Desneux et al. 2007 ; Müller 2018 ). Given that both synthetic and botanical insecticides, as well as biological control utilizing D. luteipes , are considered essential tools for S. frugiperda management in food production systems, this study tested the following hypotheses: (I) residues of botanical and synthetic insecticides may impact D. luteipes differentially across its life stages, (II) affect its behavior, and (III) cause transgenerational effects. Identifying selective products is fundamental to advancing the integrated management of S. frugiperda while safeguarding D. luteipes. Materials and methods Insect rearing Adults of D. luteipes were collected from corn crops without insecticide application in an experimental field in Piracicaba, São Paulo, Brazil (22°42'49.1"S 47°37'32.8"W). Plastic containers (25.5 cm long × 18.5 cm wide × 8 cm high) covered with organza fabric and brown paper were used for laboratory maintenance. Inside the containers, accordion paper was provided as a refuge and shelter. Both adults and nymphs were fed ad libitum with an artificial diet developed by Guimarães et al. ( 2006 ), consisting of cat food (35%), wheat germ (27%), brewer's yeast (23%), powdered milk (14%), Nipagin (0.5%), and ascorbic acid (0.5%). Plastic straws (0.8 cm diameter) containing moistened cotton were used as substrates for oviposition (Naranjo-Guevara et al. 2017 ). As this species exhibits parental care, females were transferred with their respective eggs to new containers after oviposition. They remained there for fourteen days before being reintegrated into the colony. The nymphs were kept separate until adult emergence, with some used in experiments and others reserved for colony maintenance. The insects used in the bioassays belonged to the 14th laboratory-reared generations. Spodoptera frugiperda larvae were obtained from a susceptible population maintained in the laboratory for over 20 years. The pupae and adults were kept in cages made of PVC tubes (20 cm in diameter × 20 cm in height), internally lined with white paper to facilitate oviposition. Neonate larvae were reared in 100 mL plastic cups containing an artificial diet (Greene et al. 1976 ). Upon reaching the third instar, they were individualized and kept until the pupal stage, at this point, they were transferred back to the cages. Adults were fed a 10% honey solution. All insect rearing and experiments were conducted in a climate-controlled room (temperature: 25 ± 1°C, relative humidity: 60 ± 10%, and photoperiod: 12 L:12 D). Obtaining the treatments The treatments involved two non-commercial botanical pre-formulations and three commercial insecticides, which consisted of two botanical and one organosynthetic. The pre-formulations included (1) an aqueous emulsion of the methanolic fraction from the ethanolic extract of Annona montana leaves (EFAMON) and (2) an aqueous emulsion of the ethanolic extract from Annona mucosa seeds (ESAM). The commercial insecticides comprised (1) Anosom® 1 EC, a botanical product based on acetogenins (annonin) (AgriLife SOM Phytopharma Ltda., Hyderabad, India); (2) Azamax® 1.2 EC, also a botanical insecticide containing limonoids (azadirachtin and 3-tigloylazadirachtol) (UPL Brasil Ltda., Campinas, São Paulo, Brazil); and (3) Premio® 200 SC, an organosynthetic insecticide with chlorantraniliprole as the active ingredient (FMC Química do Brasil Ltda., Campinas, São Paulo, Brazil). Distilled water and the solvents used in the pre-formulations were the control group. Preparation of botanical pre-formulations Botanical pre-formulations were prepared using ethanolic extracts from A. montana leaves and A. mucosa seeds. The leaves and seeds were dried in an oven at 38°C for 48h, ground in a knife mill, and the resulting powder was extracted with ethanol. After three days of rest, the material was filtered, and the solvent was removed in a rotary evaporator at 50°C and − 600 mmHg. The A. montana extract was then subjected to liquid-liquid partition to separate phases with different chemical affinities and obtain the methanolic fraction, according to the procedure described by Lima et al. ( 2022 ). Emulsions of the methanolic fraction of A. montana and the ethanolic extract of A. mucosa were prepared by adding the surfactants Triton® X-100 (0.1%, v v − 1 ) and Tween® 80 (1%, v v − 1 ), along with a mixture (1%, v v − 1 ) of acetone and methanol (1:1, v v − 1 ). These components helped to break the surface tension of the water, improve leaf adhesion, and facilitate the dilution of the emulsions. Lethal concentration (LC) of S. frugiperda Concentration-response curves were performed to determine the lethal concentration of treatments required to kill the pest S. frugiperda . Different treatment concentrations (at least eight) were incorporated into 100 g of artificial diet. After preparation, 1 mL of the contaminated diet was distributed into wells of 128-cell plastic plates (Advento do Brasil, São Paulo, Brazil) using a hypodermic syringe (BD PlastipaK™). The plates were infested with neonate larvae (< 24 hours old) and sealed with transparent plastic lids for aeration. Mortality was assessed daily over seven days. For the EFAMON treatment, the concentrations, before being added to the diet, were pre-diluted in 6 mL of acetone and methanol (1:1, v/v). These same solvents were used in the control treatment. A completely randomized design was adopted, with four replicates per treatment and 16 insects per replicate. For the ESAM and Anosom®, as their concentration-response curves (LC) for S. frugiperda had already been determined in previous studies a mortality bioassay was conducted to confirm these values (ESAM LC 90 = 1,386.0 mg kg − 1 ; Anosom® LC 90 = 2,959.0 mg kg − 1 ) (Ansante et al. 2015 , 2017 ). The bioassay followed the same procedures described above, confirming the toxicity of these two treatments against the pest. Selectivity bioassays on Doru luteipes Selectivity bioassays were conducted to assess the lethal and sublethal effects of treatments on Doru luteipes . The predator was exposed to tarsal contact with leaves treated with the lethal concentration (LC 90 ) previously determined for the pest. All experiments were performed in a completely randomized design and maintained in a climate-controlled room (temperature: 25 ± 1°C, relative humidity: 60 ± 10%, and a photoperiod of 12 L: 12 D h). Lethal effect on developmental stages To evaluate the lethal effect of treatments on D. luteipes mortality, corn leaf discs (vegetative stage, V5) with 4.5 cm diameter were cut and dipped in the treatment solutions for 10 seconds. Distilled water and the solvents from pre-formulations were used as a control. After drying, the discs were placed in plastic containers (4.5 cm diameter and 5.0 cm height) containing carrageenan (2.5%, w v − 1 ) at the base to maintain moisture. Subsequently, insects were grouped by developmental stage (1st, 2nd, 3rd, 4th instars, and adults), all 24 hours old, and placed in containers containing treated leaves to allow tarsal contact with the treatments. An artificial diet was provided for feeding, along with moistened cotton to maintain adequate humidity. The containers were sealed with perforated lids to allow aeration, and mortality was recorded 48 hours after exposure. Each treatment consisted of five replicates, with six insects per replicate (three males and three females for the adult stage). Sublethal effects Predation and walking behavior For the sublethal effects assessment, adult D. luteipes were exposed to the LC 90 concentration of the treatments for 24 hours, following the same procedure described previously. This concentration was chosen because no significant mortality was observed in adults during the lethal effect bioassay. After exposure, to evaluate predation, each insect was individually transferred to a plastic container (4.5 cm in diameter × 6.5 cm in height) and provided with 20 first-instar larvae of Spodoptera frugiperda . After 12 hours, the number of preyed larvae was recorded. The experiment included six treatments, ten replicates per treatment, consisting of five males and five females, with one insect per replicate, meaning one adult for every 20 larvae of S. frugiperda . All adults used in the experiment were no more than 24 hours old and had not received any artificial diet before the test. The behavioral bioassay aimed to assess whether the treatments affected the movement activity of the insects. Each experimental unit consisted of four adult insects kept in plastic containers (25.5 cm length × 18.5 cm width × 8 cm height). After the exposure period (24h), each replicate was filmed for 10 minutes using a Sony Handycam camcorder (Hdr-cx405 Full Hd) positioned perpendicular to the insect container. The ambient light was covered with red cellophane. A total of six replicates per treatment were performed. Movement data were analyzed using an automated image capture system (EthoVision, Noldus et al. 2001 ). The variables analyzed were “Distance moved” (cm) and “Velocity” (cm s − 1 ). “Distance moved” was defined as the distance traveled by the subject's center of mass from the previous to the current sample. “Velocity” was defined as the distance traveled by the subject's center of mass per unit time (Cann et al. 2013 ). Both experiments were conducted at night (from 7 pm to 9 pm) when D. luteipes exhibits increased predatory activity (Naranjo-Guevara et al. 2017 ). Biological parameters and transgenerational effects To evaluate the sublethal effects of treatments on the biological parameters of D. luteipes , newly emerged adults (less than 24 hours old) were exposed to treated leaves for 24 hours. After exposure, ten couples/treatment were formed and placed individually in containers containing an artificial diet and moistened cotton. Daily observations recorded longevity and reproductive parameters, including the pre-oviposition period and fecundity. Once the females laid their eggs, the males were separated until the nymphs hatched, as D. luteipes exhibit parental care, and the presence of males could stress females during this period. From these couples, 10 egg masses (30 eggs per mass) were selected to assess the development, viability, and sex ratio of the F 1 generation. The number of males and females was determined by differentiating the cerci: more curved cerci indicate males, while straight cerci indicate females. Subsequently, a fertility life table was constructed to investigate the effects of the treatment on the population growth. Biological data were collected, including x = average age of insects from egg stage, lx = survival rate, mx = specific fertility, and lx.mx = total number of females born at age x . These data were used to estimate the life table parameters: net reproductive rate ( R 0 ), mean generation time ( T ), intrinsic rate of increase ( r m ), and finite rate of population increase ( λ ) (Maia et al. 2014 ). The experiment included six treatments, each with 10 replicates (one pair per replicate). Ten egg masses/couples containing 30 eggs each were used to assess egg cohorts. Statistical analyses The mortality data of developmental stages and predation capacity were analyzed by fitting a Generalized Linear Model (GLM) assuming binomial distribution. Behavior data were analyzed by fitting GLM with Gaussian distribution. In contrast, longevity, pre-oviposition period, fecundity, F 1 generation development, viability, and sexual ratio data were analyzed using GLM with Poisson distribution, with correction for overdispersion when necessary. For all models, the fit quality was assessed using a half-normal plot with simulated envelopes at the 95% level (Moral et al. 2017 ). The fertility life table was constructed using the lifetable.R procedure described by Maia et al. ( 2014 ) using the Jackknife method, and parameters were analyzed using GLM with Gaussian distribution. For all fitted models, the deviance analysis was conducted, and when necessary, means were compared using Tukey's test ( p < 0.05). All analyses were performed using R statistical software version 4.2.1 (R Core Team, 2021 ; http://www.R-project.org ). Results Lethal concentration (LC) of S. frugiperda The lethal concentration (LC) required for the non-commercial botanical pre-formulation EFAMON to cause 90% mortality in Spodoptera frugiperda larvae was 10,949.05 mg kg⁻¹ (Table 1 , Fig. 1 a). Among the commercial insecticides, the botanical product Azamax® (azadirachtin + 3-tigloylazadirachtol) showed an LC 90 of 65.429 mg kg⁻¹, while the synthetic insecticide Premio® (chlorantraniliprole) exhibited the lowest LC 90 value, 0.433 mg kg⁻¹ (Table 1 , Fig. 1 a). The toxicity bioassay confirmed that the lethal concentrations of the botanical pre-formulation ESAM (LC 90 = 1,386.0 mg kg⁻¹) and the botanical insecticide Anosom® (LC 90 = 2,959.0 mg kg⁻¹) effectively caused 90% mortality in the pest population (Fig. 1 b). Table 1 Lethal concentrations (LC 50 and LC 90 ) of botanical and synthetic insecticides for Spodoptera frugiperda larvae seven days after exposure Treatments N b LC 50 (mg kg − 1 ) (95% CI c ) LC 90 (95% CI) Slope ± SE d χ 2 (df e ) P Pre-formulation EFAMON a 452 2,440.70 (1.960,76-3.038,12) 10,949.05 (8,115.53-14,771,89) 1.93 ± 0.20 9.39 (5) 0.094 Azamax® EC, 1.2g a.i L − 1 (Azadirachtin + 3-tigloylazadirachtol) 442 10.619 (8.668–13.010) 65.429 (44.279–96.680) 1.62 ± 0.16 8.04 (4) 0.090 Premio® SC, 200g a.i. L − 1 (Chlorantraniliprole) 523 0.176 (0.154–0.201) 0.433 (0.371–0.506) 3.28 ± 0.28 2.58 (4) 0.630 a EFAMON = Aqueous emulsion of the methanolic fraction of the ethanolic extract of Annona montana leaves. b N = Number of tested S. frugiperda . c CI = Confidence Interval at 95% error probability. d SE = Standard Error. e df = Degrees of freedom Lethal effect on developmental stages The treatments affected the survival of D. luteipes at all nymphal stages (χ²= 46.633, df = 20;120, p < 0.001) (Fig. 2 ). Premio® (chlorantraniliprole) caused the highest mortality, with values above 90% in the first instar and over 50% in other instars. However, this effect did not differ from that of ESAM (aqueous emulsion of the ethanolic extract of Annona mucosa seeds) and Anosom® (acetogenin annonin ) in the first instar. For nymphs in the 2nd to 4th instars, botanical insecticides resulted in mortality below 30%. The tested treatments did not significantly affect mortality in the adult stage (F = 1.547, df = 5;120, p = 0.1804) (Fig. 2 ). Predation and walking behavior The interaction between the sex of adults and treatments was not significant (F = 0.988, df = 5;48, p = 0.435); however, the average predation capacity of males was higher than that of females (F = 16.536, df = 1;48, p < 0.001), with males preying on 89% and females on 77% of the prey offered. Regarding the treatments, there were differences in the predation of S. frugiperda by D. luteipes (F = 33.967, df = 5;48, p < 0.001), with adults exposed to leaves treated with the insecticide Premio® showing the lowest predation rate (40.5%). In comparison, predation was higher than 86% for other treatments, unlike the control with 92% predation (Fig. 3 ). The walking behavior of adult D. luteipes was affected by the treatments, with analysis showing effects on velocity (F = 4.89, df = 5;63, p < 0.001) and distance (F = 3.506, df = 5;63, p < 0.01) (Fig. 4). A similar pattern was observed for both the “Velocity” and “Distance moved” variables, as expected due to the relationship between the variables. The adults contaminated with the synthetic insecticide Premio® exhibited lower locomotor activity, covering shorter distances (433.97 cm) and walking at a slower velocity (0.73 cm s − 1 ). However, compared to the other treatments, no significant differences in velocity were found between the synthetic insecticide Premio® (0.73 cm s − 1 ) and the commercial botanical insecticide Anosom® (0.98 cm s − 1 ) (Fig. 4a). No significant differences were observed in the distance moved between Premio® (433.97 cm), Anosom® (570.33 cm), and the negative control group (566.10 cm) (Fig. 4b). Fig 4 Means (± SE) of velocity (a) and distance moved (b) traveled by adult D. luteipes exposed to synthetic and botanical insecticides. Different letters among treatments indicate significant differences (Tukey, p < 0.05). EFAMON (aqueous emulsion of the methanolic fraction of the ethanolic extract of Annona montana leaves); ESAM (aqueous emulsion of the ethanolic extract of Annona mucosa seeds); Anosom ® (acetogenin annonin); Azamax ® (azadirachtin + 3-tigloylazadirachtol); Premio ® (chlorantraniliprole) Influence on longevity and reproductive parameters Adults exposed to leaves contaminated with the treatments for 24 h showed differences in longevity (Table 2 ). The treatments constituted by ESAM and the synthetic insecticide Premio® reduced adult longevity to 88.88 and 95.17 days, respectively, differing from the control, which was 121.6 days. However, they did not differ from those of the other tested treatments. A similar pattern was observed for males, where Premio® reduced longevity to 71.56 days, differing from the control group, which was 112 days. Table 2 Mean longevity (± SE) of adult D. luteipes after exposure to synthetic and botanical insecticides Treatments Longevity (days) Adult Male Female Control 121.6 ± 4.75a 112.1 ± 6.83a 133.5 ± 3.48a EFAMON 115.7 ± 5.97ab 106.7 ± 7.77ab 124.7 ± 8.22ab ESAM 88.88 ± 6.78c 86.90 ± 9.47c 91.38 ± 10.3ab Anosom® 105.3 ± 4.85abc 102.3 ± 6.8abc 108.4 ± 7.16ab Azamax® 99.00 ± 5.67abc 104.1 ± 10.16bc 93.33 ± 4.06ab Premio® 95.17 ± 8.50bc 71.56 ± 7.5abc 121.7 ± 9.41b F 4.00 3.34 5.15 p < 0.01 < 0.05 < 0.001 Means followed by the same letter in the column do not differ statistically (Tukey, p < 0.05). EFAMON (aqueous emulsion of the methanolic fraction of the ethanolic extract of Annona montana leaves); ESAM (aqueous emulsion of the ethanolic extract of Annona mucosa seeds); Anosom® (acetogenin annonin); Azamax® (azadirachtin + 3-tigloylazadirachtol); Premio® (chlorantraniliprole) Among the reproductive parameters assessed, the pre-oviposition period was influenced by the treatments, with synthetic insecticide Premio® resulting in the shortest pre-oviposition period (9.44 days) compared to the control (13.10 days) and ESAM (13.00 days), indicating rapid sexual maturation of females exposed to this diamide. However, it did not differ statistically from botanical insecticides based on acetogenins (EFAMON and Anosom®) and limonoids (Azamax®). Mean fecundity values ranged from 31.20 to 57.10, with no significant statistical differences observed among the treatments (Table 3 ). Table 3 Effects of synthetic and botanical insecticides on the reproductive parameters of D. luteipes Treatments Reproductive parameters Pre-oviposition (days) Fecundity (eggs/female) Control 13.10 ± 0.54a 53.30 ± 8.75a EFAMON 12.00 ± 0.70ab 53.10 ± 9.26a ESAM 13.00 ± 1.21a 31.20 ± 10.37a Anosom® 12.44 ± 0.80ab 39.30 ± 7.89a Azamax® 11.00 ± 0.57ab 46.20 ± 5.98a Premio® 9.44 ± 1.00b 57.10 ± 9.00a F 3.14 1.56 p < 0.05 0.18 Means followed (± SE) by the same letter in the column do not differ statistically from each other (Tukey p < 0.05). EFAMON (aqueous emulsion of the methanolic fraction of the ethanolic extract of Annona montana leaves); ESAM (aqueous emulsion of the ethanolic extract of Annona mucosa seeds); Anosom® (acetogenin annonin); Azamax® (azadirachtin + 3-tigloylazadirachtol); Premio® (chlorantraniliprole) Biological parameters and transgenerational effects The treatments did not affect the development time and sex ratio of the F 1 generation. The egg incubation and first- and fourth-instar nymph durations were approximately 8 days, while second- and third-instar nymphs lasted about 6 days. The complete cycle, from egg to adult, spanned 36–37 days, with a balanced sex ratio (close to 0.5) (Table 4 ). However, the viability of fourth-instar nymphs was affected by the treatments. EFAMON resulted in the lowest viability (54.54%), significantly lower than the control (91.91%), Anosom® (93.56%), and Premio® (86.87%) (Table 5 ). The treatments also influenced the demographic parameters highlighted in the fertility life table (Table 6 ). Anosom® presented the lowest intrinsic rate of growth ( rₘ = 0.039), significantly lower than the control (0.05), Azamax® (0.058), and Premio® (0.052). The net reproductive rate ( R 0 ) increased in the following order: Anosom® (8.68), EFAMON (9.82), ESAM (10.64), control (15.77), Premio® (17.61), and Azamax® (21.66). A similar pattern was observed for the finite rate of increase ( λ ). No statistical differences were observed for the mean generation time ( T ). Table 4 Mean (± SE) development time and sex ratio of the F 1 generation of D. luteipes exposed to synthetic and botanical insecticides Treatments Time development (days) Sexual Ratio Egg 1st 2nd 3rd 4th Egg-adult Control 8.65 ± 0.18 8.00 ± 0.26 5.50 ± 0.26 6.37 ± 0.37 8.00 ± 0.32 36.50 ± 0.53 0.51 ± 0.05 EFAMON 8.62 ± 0.18 8.25 ± 0.16 6.14 ± 0.26 6.57 ± 0.52 7.20 ± 0.37 37.66 ± 0.84 0.61 ± 0.06 ESAM 8.5 ± 0.22 8.5 ± 0.22 6.0 ± 0.36 6.6 ± 0.49 7.83 ± 0.30 37.5 ± 0.5 0.51 ± 0.07 Anosom® 8.85 ± 0.14 8.57 ± 0.29 6.00 ± 0.21 5.85 ± 0.26 8.00 ± 0.30 37.28 ± 0.47 0.47 ± 0.04 Azamax® 8.50 ± 0.18 8.62 ± 0.18 5.25 ± 0.31 6.25 ± 0.31 8.00 ± 0.37 36.65 ± 0.26 0.52 ± 0.06 Premio® 8.42 ± 0.20 8.28 ± 0.18 5.71 ± 0.18 6.33 ± 0.33 7.16 ± 0.47 36.00 ± 0.25 0.51 ± 0.21 F 0.62 1.17 1.63 0.52 1.13 1.58 0.46 p 0.68 0.34 0.17 0.76 0.36 0.19 0.80 EFAMON (aqueous emulsion of the methanolic fraction of the ethanolic extract of Annona montana leaves); ESAM (aqueous emulsion of the ethanolic extract of Annona mucosa seeds); Anosom® (acetogenin annonin); Azamax® (azadirachtin + 3-tigloylazadirachtol); Premio® (chlorantraniliprole) Table 5 Viability (%) of eggs and immature stages of the F 1 generation of D. luteipes exposed to synthetic and botanical insecticides Treatments Viability (%) Egg 1st 2nd 3rd 4th Total Control 73.41 ± 7.23 87.01 ± 4.56 91.83 ± 3.12 95.52 ± 2.13 91.91 ± 4.76a 52.747.76 EFAMON 69.46 ± 6.60 89.68 ± 3.97 91.62 ± 3.60 76.46 ± 12.85 54.54 ± 11.50b 27.27 ± 8.25 ESAM 87.34 ± 5.50 86.31 ± 10.41 88.05 ± 4.12 84.07 ± 3.07 74.36 ± 5.96ab 39.5 ± 4.82 Anosom® 55.76 ± 11.76 91.29 ± 3.23 96.08 ± 1.74 97.17 ± 2.06 93.56 ± 4.78a 46.51 ± 11.35 Azamax® 77.29 ± 7.73 85.58 ± 4.46 96.91 ± 1.72 89.18 ± 4.67 74.31 ± 5.33ab 41.34 ± 5.18 Premio® 88.49 ± 6.58 90.92 ± 4.12 84.38 ± 5.40 85.71 ± 14.29 86.87 ± 6.32a 53.84 ± 12.81 F 2.24 0.22 1.92 0.89 4.74 1.30 p 0.07 0.95 0.11 0.49 < 0.01 0.28 Means (± SE) followed by the same letter in the column do not differ statistically from each other (Tukey p < 0.05). EFAMON (aqueous emulsion of the methanolic fraction of the ethanolic extract of Annona montana leaves); ESAM (aqueous emulsion of the ethanolic extract of Annona mucosa seeds); Anosom® (acetogenin annonin); Azamax® (azadirachtin + 3-tigloylazadirachtol); Premio® (chlorantraniliprole) Table 6 Population parameters of D. luteipes (F 1 ) originated from adults exposed to botanical and synthetic insecticides Treatments Demographic parameter r m R 0 T λ Control 0.050 ± 0.001ab 15.77 ± 1.70abc 55.183 ± 1.041a 1.051 ± 0.001ab EFAMON 0.042 ± 0.002bc 9.82 ± 1.33c 54.603 ± 1.397a 1.043 ± 0.002bc ESAM 0.041 ± 0.002bc 10.64 ± 2.11bc 58.310 ± 2.29a 1.042 ± 0.002bc Anosom® 0.039 ± 0.003c 8.68 ± 1.74c 55.809 ± 2.141a 1.040 ± 0.004c Azamax® 0.058 ± 0.001a 21.66 ± 1.70a 53.025 ± 0.87a 1.060 ± 0.001a Premio® 0.052 ± 0.002a 17.61 ± 1.98ab 55.051 ± 1.263a 1.054 ± 0.002a F 11.85 8.66 1.03 11.99 p < 0.001 < 0.001 0.41 < 0.001 Means (± SE) followed by the same letter in the column do not differ statistically from each other (Tukey p < 0.05). ( r m = intrinsic rate of increase, R 0 = net reproductive rate, T = mean generation time and λ = finite rate of population increase). EFAMON (aqueous emulsion of the methanolic fraction of the ethanolic extract of Annona montana leaves); ESAM (aqueous emulsion of the ethanolic extract of Annona mucosa seeds); Anosom® (acetogenin annonin); Azamax® (azadirachtin + 3-tigloylazadirachtol); Premio® (chlorantraniliprole) Discussion This study provides significant contributions to the understanding of the selectivity of botanical and organosynthetic insecticides on the predator D. luteipes . The synthetic insecticide Premio® (chlorantraniliprole) was found to cause high mortality in nymphs, an effect that was not observed in adults. Insecticide tolerance can vary significantly depending on insect’s life stage. The immature stages of natural enemies tend to be more susceptible (Stecca et al. 2017; Freitas et al. 2017 ; Musa et al. 2021 ; Potin et al. 2022 ). This observation can be explained by two factors: 1) the higher ability of the insecticide to penetrate the bodies of nymphs, as their exoskeletons are less sclerotized compared to that of adults (Andersen 2010 , 2012 ; Pang et al. 2023 ); 2) the high metabolic cost of detoxifying xenobiotics (Müller 2018 ; Khan et al. 2021 ). Insects have detoxification mechanisms to eliminate harmful compounds; however, nymphs may compromise vital resources for their physiological survival by allocating energy to detoxification (Ferreira et al. 2013 ; Luong and Horn 2017 ; Khan et al. 2021 ). In a similar study conducted by Freitas et al. ( 2017 ), it was observed that nymphs (1st, 2nd, and 4th instars) of D. luteipes exposed to chlorantraniliprole residues at the label-recommended concentration had their survival affected, which is consistent with the results of our study. Another study by Campos et al. ( 2011 ) demonstrated that chlorantraniliprole does not cause adult mortality. In another species of Dermaptera, Euborelia annulipes , chlorantraniliprole showed no toxicity in either adult or third-instar nymphs (Potin et al. 2022 ). The botanical insecticides ESAM (aqueous emulsion of the ethanolic extract of Annona mucosa seeds) and Anosom® (acetogenin annonin) caused high mortality in first-instar nymphs. These two botanical insecticides are derived from plants of the Annonaceae family, known for biosynthesizing acetogenins (ACGs), which have documented insecticidal activities against various pest insect species (Ansante et al. 2015 , 2017 ; Ribeiro, et al. 2015 ; Souza et al. 2017 ; Gomes 2018 ; Hidalgoa et al. 2020 ). Their modes of action include inhibiting complex I of the mitochondrial electron transport system, preventing ATP production, and induction of programmed cell death (Alali et al. 1999 ; Tormo et al. 1999 ). Recent studies have also demonstrated the effects of acetogenins on the digestive system of certain insects, reducing nutrient absorption (Costa et al. 2016 ; Machado et al. 2021 ). Additionally, the interaction of acetogenins with cell membrane phosphates represents a novel site of action, leading to dehydration and causing irreversible damage to their structure and biological functions (Bombasaro et al. 2011 ; Blessing et al. 2012). Thus, first-instar nymphs may be more vulnerable to these compounds due to their lower exoskeleton sclerotization and high metabolic demand for detoxification, which may explain the higher observed mortality (Andersen 2010 , 2012 ; Ferreira et al. 2013 ; Müller 2018 ; Pang et al. 2023 ). Evaluating the sublethal impact of insecticides on the predation capacity and locomotion behavior of predators ensures that these biological control agents can continue to fulfill their ecological roles (Desneux et al. 2007 ). Although the survival of adult D. luteipes was not affected by the treatments, the synthetic insecticide Premio® (chlorantraniliprole) significantly reduced prey consumption and walking velocity. Predation is the primary ecological function of these insects, and changes in locomotion behavior may compromise their predatory efficacy, negatively affecting pest control capabilities (Campos et al. 2011 ; Freitas et al. 2017 ; He et al. 2019 ; Moreira et al. 2023 ; Silva et al. 2023 ). Chlorantraniliprole is a ryanodine receptor modulator that affects muscle calcium release (Nauen 2006 ; Lahm et al. 2009 ). This insecticide can impact all muscles, including those related to locomotion, thus affecting insect movement and, consequently, their predation capability (He et al. 2019 ). Similar outcomes were observed in a study by Freitas et al. ( 2017 ), where the locomotion behavior of D. luteipes was reduced following exposure to chlorantraniliprole. Other studies support our findings regarding predation capacity. In Euborellia annulipes (Dermaptera: Anisolabididae), predation significantly decreases after chlorantraniliprole exposure (Potin et al. 2022 ). This impairment has also been observed in other natural enemies (Musa et al. 2021 ; Moreira et al. 2023 ). In contrast, Campos et al. ( 2011 ) showed that this insecticide does not affect the predation capacity of D. luteipes . The botanical insecticide ESAM (aqueous emulsion of the ethanolic extract of Annona mucosa seeds) and Premio® (chlorantraniliprole) reduced the average longevity of adults. Regarding reproductive parameters, Premio® accelerated the pre-oviposition period, whereas fecundity was unaffected by any treatment. Literature suggests that reproduction is an energetically costly activity (Tallamy and Denno 1982 ; Soulages 2010 ; De Loof 2011 ). In this study, the number of eggs per female was not influenced; however, insects exposed to ESAM and Premio® had shorter lives. This suggests a possible trade-off: insects exposed to these compounds had their physiological survival activities affected while maintaining reproductive capacity (Blacher et al. 2017 ; Jiang et al. 2023 ). Additionally, the stress caused by Premio® may accelerate the reproductive cycle in females. Similarly, this stress might respond to the toxic environment, inducing females to oviposit earlier as a survival strategy without necessarily reducing their total egg production (Fogel et al. 2016 ; Sial et al. 2018 ; Azhar and Khan 2024 ). Freitas et al. ( 2017 ) demonstrated that only 20% of D. luteipes adults that came into contact with chlorantraniliprole residues survived up to 50 days. Other predators, such as Chrysoperla spp., also had their longevity affected by this insecticide (Wankhade et al. 2020 ). However, chlorantraniliprole did not affect the fecundity of Coccinella septempunctata (Coleoptera: Coccinellidae) at the lowest tested dose (Cong et al. 2023 ). Similar results were obtained for Coleomegilla quadrifasciata (Coleoptera: Coccinellidae) when exposed to dry chlorantraniliprole residues (Silva et al. 2020 ). In contrast, He et al. ( 2019 ) observed that applying the recommended field dose of chlorantraniliprole to C. septempunctata reduced fecundity. These results indicate that for D. luteipes , the lethal concentration (LC 90 ) of chlorantraniliprole-based insecticide used in this study did not cause changes in fecundity. In contrast, the effects may differ for other predator groups. In addition to the direct impacts of insecticides, the effects of previous exposure can be transmitted to subsequent generations (Cheng et al. 2022 ; Afza et al. 2023 ). Therefore, selectivity studies must include an evaluation of the transgenerational effects (Le et al. 2021 ; Moreira et al. 2023 ). In this study, parameters such as developmental time, viability of developmental stages, sex ratio, and demographic parameters of the F 1 generation were evaluated. The development time of each stage of D. luteipes and sex ratio were not influenced by the treatments. Similar results were found by Potin et al. ( 2022 ), who studied the effect of chlorantraniliprole on Euborellia annulipes (Dermaptera: Anisolabididae) and observed no impact on development time. Additionally, Abreu et al. ( 2024 ) investigated the selectivity of different aqueous extracts on the duration and fecundity of Marava arachidis (Dermaptera: Labiidae) and demonstrated that, at a concentration of 10% (w v − 1 ), the extracts did not affect this species. Only the viability of the fourth-instar nymphs was influenced by the treatments, with the botanical insecticide EFAMON causing the lowest viability. No study has demonstrated the effects of A. montana derivatives on natural enemies. However, this plant belongs to the same genus as other Annona species, whose extracts have been shown to affect the viability of various insect species (Bernardi et al. 2017 ; Souza et al. 2019 ; Gonçalves et al. 2021 ). Much of this effect is attributed to the compounds in its composition, such as alkaloids, acetogenins, triterpenes, steroids, and lignans. Among these, acetogenins are particularly noteworthy, with their possible modes of action described earlier in this study (Gomes 2018 ; Hidalgoa et al. 2020 ). One approach to assess the impact of insecticides on insect population dynamics is to use fertility life tables (Amarasekare et al. 2016 ; Rossini et al. 2024 ). This study revealed that the F 1 generation, whose parents were exposed to Anosom® (acetogenin annonin) treatment, showed lower values of intrinsic growth rate ( r m ) and finite rate of increase ( λ ) than the control. These parameters consider data on female fecundity and survival, which may indicate potential future effects on population dynamics, although not statistically different in this study (Kakde et al. 2014 ). The intrinsic population growth rate ( r m ) reflects the maximum growth rate of a population, with higher values indicating a more significant potential for population success. The finite rate of increase represents the population growth rate from one generation to the next, and both parameters indicate whether the population is growing, stable, or declining (Maia et al. 2000 ). A similar result was observed by Morais ( 2020 ), who demonstrated a reduction in the fecundity of the predator Cryptolaemus montrouzieri (Coleoptera: Coccinellidae) when exposed to the same treatment. This suggests that Anosom® may have significant effects on population dynamics. The results of this study indicate that the botanical insecticides, particularly a formulation based on limonoids (Azamax®) and an emulsion of the methanolic fraction of the ethanolic extract of Annona montana leaves (EFAMON), are less lethal to the natural enemy D. luteipes than synthetic insecticide chlorantraniliprole (Premio®). Chlorantraniliprole exhibited high toxicity, negatively impacting the mortality, predation capacity, and walking behavior of D. luteipes . These findings suggest that the botanical insecticides tested may be more compatible with conserving the studied natural enemy. However, there is no simple answer when it comes to selectivity studies. While botanical insecticides have demonstrated reduced effects on certain parameters, the results have varied for others. This lack of a definitive response is expected, as selectivity studies are complementary and build upon each other. Future investigations, particularly ecotoxicological assessments conducted under field conditions, can provide a more comprehensive understanding based on the results obtained. Therefore, the findings of this research offer significant contributions to filling the gaps in compatibility between chemical and biological control, promoting more sustainable agricultural practices. Declarations Author contributions EDRS: conceptualization, methodology, statistical analysis, writing original draft; LVT: methodology, statistical analysis; MY, GSR, and IB: methodology and review; PTY: conceptualization, writing review and editing; LPR: writing review and editing. All authors reviewed and approved the manuscript . Funding This research was funded by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) – Finance code 001. Conflict of interest The authors declare no competing interests Ethics approval Not applicable References Abreu KG, Brito CH de, Filho MC de O et al (2024) Physiological selectivity of aqueous extracts on nymphs and adults of Marava arachidis (Dermaptera: Labiidae). Rev Principia - Divulg Científica e Tecnológica do IFPB. https://doi.org/doi:http://dx.doi.org/10.18265/1517-0306a2022id7259. Afza R, Afzal A, Riaz MA et al (2023) Sublethal and transgenerational effects of synthetic insecticides on the biological parameters and functional response of Coccinella septempunctata (Coleoptera : Coccinellidae) under laboratory conditions. Front Physiol 14:1–14. https://doi.org/10.3389/fphys.2023.1088712 Alali FQ, Liu X, Mclaughlin JL (1999) Annonaceous Acetogenins : Recent Progress. 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Dissertation, Universidade Federal de Lavras Pang R, Chen B, Wang S et al (2023) Decreased cuticular penetration minimizes the impact of the pyrethroid insecticide λ-cyhalothrin on the insect predator Eocanthecona furcellata . Ecotoxicol Environ Saf 249:114369. https://doi.org/10.1016/j.ecoenv.2022.114369 Pasini A, Parra JRP, Nava DE, Butnariu AR (2010) Exigências térmicas de Doru lineare Eschs. e Doru luteipes Scudder em laboratório. Ciência Rural 40:1562–1568. https://doi.org/10.1590/s0103-84782010000700013 Potin DM, Machado AVA, Barbosa PRR, Torres JB (2022) Multiple factors mediate insecticide toxicity to a key predator for cotton insect pest management. Ecotoxicology 490–502. https://doi.org/10.1007/s10646-022-02526-6 R Core Team (2021) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/ Rezende-Teixeira P, Dusi RG, Jimenez PC et al (2022) What can we learn from commercial insecticides? Efficacy, toxicity, environmental impacts, and future developments. Environ Pollut 300:118983. https://doi.org/10.1016/j.envpol.2022.118983 Ribeiro, Leandro Do Prado, Santos MS, Gonçalves GLP, Vendramim JD (2015) Toxicity of an Acetogenin-Based Bioinsecticide Against Diaphorina citri (Hemiptera: Liviidae) and its Parasitoid Tamarixia radiata (Hymenoptera: Eulophidae). Florida Entomol 98:835–842. https://doi.org/https://doi.org/10.1653/024.098.0304 Romero Sueldo GM, Virila EG (2009) Datos biológicos de Doru luteipes (Dermaptera: Forficulidae) en plantaciones de caña de azúcar y consumo de huevos de Diatraea saccharalis (Lepidoptera: Crambidae) en condiciones de laboratorio. Rev la Soc Entomológica Argentina 68:359–363 Romero Sueldo M, Dode M, Virla EG (2014) Depredación de Doru luteipes y D. lineare (Dermaptera: Forficulidae) sobre Rhopalosiphum maidis (Hemiptera: Aphididae) en condiciones de laboratorio. 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J Pest Sci (2004) 90:701–709. https://doi.org/10.1007/s10340-016-0817-9 Souza CM de, Baldin ELL, Ribeiro LP et al (2019) Antifeedant and growth inhibitory effects of Annonaceae derivatives on Helicoverpa armigera (Hübner). Crop Prot 121:45–50. https://doi.org/10.1016/j.cropro.2019.03.008 Sparks TC, Bryant RJ (2022) Innovation in insecticide discovery: Approaches to the discovery of new classes of insecticides. Pest Manag Sci 78:3226–3247. https://doi.org/10.1002/ps.6942 Tallamy DW, Denno RF (1982) Life History Trade-Offs in Gargaphia Solani (Hemiptera : Tingidae): The Cost of Reproduction. Ecology 63:616–620 Tay WT, Meagher RL, Czepak C, Groot AT (2023) Spodoptera frugiperda : Ecology, Evolution, and Management Options of an Invasive Species. Annu Rev Entomol 68:299–317. https://doi.org/10.1146/annurev-ento-120220-102548 Tormo JR, Gallardo T, Cortes D, Estornell E (1999) Specific interactions of monotetrahydrofuranic annonaceous acetogenins as inhibitors of mitochondrial complex I. Chem Biol Interact 122:171–183 Torres JB, Bueno ADF (2018) Conservation biological control using selective insecticides – A valuable tool for IPM. Biol Control 126:53–64. https://doi.org/10.1016/j.biocontrol.2018.07.012 Turchen LM, Golin V, Regina Butnariu A, Barbosa Pereira MJ (2014) Selectivity of Annona (Annonaceae) extract on egg parasitoid Trissolcus urichi (Hymenoptera: Platygastridae). Rev Colomb Entomol 40:176–180 Vázquez LL (2019) Climate change and biological control of pests in agriculture. In: Souza, B., Vázquez, L., Marucci R (ed) Natural Enemies of Insect Pests in Neotropical Agroecosystems. Springer, Cham, pp 63–69 Wankhade S V, Sawai HR, Chaure PR, Renuka D (2020) Comparative effects of insecticides on mortality , longevity and fecundity of Chrysoperla spp . ( Neuroptera : Chrysopidae ). J Entomol Zool Stud 8:1878–1882 Cite Share Download PDF Status: Under Review Version 1 posted Reviewers agreed at journal 23 Jan, 2025 Reviewers invited by journal 21 Jan, 2025 Editor assigned by journal 14 Jan, 2025 First submitted to journal 13 Jan, 2025 You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. We do this by developing innovative software and high quality services for the global research community. Our growing team is made up of researchers and industry professionals working together to solve the most critical problems facing scientific publishing. Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-5823057","acceptedTermsAndConditions":true,"allowDirectSubmit":false,"archivedVersions":[],"articleType":"Research Article","associatedPublications":[],"authors":[{"id":405186579,"identity":"76b80561-0c7f-466e-9b0c-3f0722b698f3","order_by":0,"name":"Emile Dayara Rabelo Santana","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAABCElEQVRIiWNgGAWjYFACxsYDDGwQ1sMPFUCKmbmBkJYGmBZmY4kzIIqRkBYGBpgWNgneNogheJXzix1uOPChzC6xf/bhBxKS82qj+duBWn5UbMOpRXJ2YsPBGeeSE2ecSzMwKNx2PHfGYcYGxp4zt3FqMbid2HCYt405seEMg0GC5LZjuQ1ALcyMbbi12IO0/G2rT5x/hv3DAd45x3LnE9JiIA3Uwth2OHHDGR7DBt6GmtwNhLRIAG052HPuuPHGMzzFzBLHDuRuBGo5iM8v/LPTHz74UVYtO+8M+/afH2rqcuedP3zwwY8K3FpgwLEBQh8GkwcIqgcCeyhdR4ziUTAKRsEoGGEAAIS6Zeo20t2XAAAAAElFTkSuQmCC","orcid":"https://orcid.org/0000-0003-1854-1385","institution":"University of Sao Paulo Luiz de Queiroz College of Agriculture: Universidade de Sao Paulo Escola Superior de Agricultura Luiz de Queiroz","correspondingAuthor":true,"prefix":"","firstName":"Emile","middleName":"Dayara Rabelo","lastName":"Santana","suffix":""},{"id":405186580,"identity":"4c55e457-057c-4b0e-a522-c0b41d40f9b4","order_by":1,"name":"Leonardo Vinicius Thiesen","email":"","orcid":"","institution":"University of Sao Paulo Luiz de Queiroz College of Agriculture: Universidade de Sao Paulo Escola Superior de Agricultura Luiz de Queiroz","correspondingAuthor":false,"prefix":"","firstName":"Leonardo","middleName":"Vinicius","lastName":"Thiesen","suffix":""},{"id":405186581,"identity":"cc35a0aa-b2d9-4fa1-b7eb-7b4642e0d8ac","order_by":2,"name":"Mariana Yamada","email":"","orcid":"","institution":"University of Sao Paulo Luiz de Queiroz College of Agriculture: Universidade de Sao Paulo Escola Superior de Agricultura Luiz de Queiroz","correspondingAuthor":false,"prefix":"","firstName":"Mariana","middleName":"","lastName":"Yamada","suffix":""},{"id":405186582,"identity":"29ea79d3-72f1-4fe5-9ea5-d3b5480deb2e","order_by":3,"name":"Gabryele Silva Ramos","email":"","orcid":"","institution":"University of Sao Paulo Luiz de Queiroz College of Agriculture: Universidade de Sao Paulo Escola Superior de Agricultura Luiz de Queiroz","correspondingAuthor":false,"prefix":"","firstName":"Gabryele","middleName":"Silva","lastName":"Ramos","suffix":""},{"id":405186583,"identity":"18056c6b-3191-4bd4-984a-65431d1c087a","order_by":4,"name":"Isabella Bueno","email":"","orcid":"","institution":"University of Sao Paulo Luiz de Queiroz College of Agriculture: Universidade de Sao Paulo Escola Superior de Agricultura Luiz de Queiroz","correspondingAuthor":false,"prefix":"","firstName":"Isabella","middleName":"","lastName":"Bueno","suffix":""},{"id":405186584,"identity":"61e936d3-7263-4621-b43c-23e66b03584a","order_by":5,"name":"Leandro do Prado Ribeiro","email":"","orcid":"","institution":"EPAGRI: Empresa de Pesquisa Agropecuaria e Extensao Rural de Santa Catarina","correspondingAuthor":false,"prefix":"","firstName":"Leandro","middleName":"do Prado","lastName":"Ribeiro","suffix":""},{"id":405186585,"identity":"861907d0-e6dd-41f3-88ba-f3e45e946490","order_by":6,"name":"Pedro Takao Yamamoto","email":"","orcid":"","institution":"University of Sao Paulo Luiz de Queiroz College of Agriculture: Universidade de Sao Paulo Escola Superior de Agricultura Luiz de Queiroz","correspondingAuthor":false,"prefix":"","firstName":"Pedro","middleName":"Takao","lastName":"Yamamoto","suffix":""}],"badges":[],"createdAt":"2025-01-14 00:59:03","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-5823057/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-5823057/v1","draftVersion":[],"editorialEvents":[],"editorialNote":"","failedWorkflow":false,"files":[{"id":74550884,"identity":"708746d7-6bca-460f-b752-965aef699d75","added_by":"auto","created_at":"2025-01-23 10:52:18","extension":"png","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":176910,"visible":true,"origin":"","legend":"\u003cp\u003eEstimated concentration-mortality curves for botanical and synthetic insecticides on \u003cem\u003eSpodoptera frugiperda\u003c/em\u003e larvae seven days after exposure \u003cstrong\u003e(a). \u003c/strong\u003eMortality (%) of \u003cem\u003eS. frugiperda\u003c/em\u003e larvae exposed to the lethal concentration (LC\u003csub\u003e90\u003c/sub\u003e) of botanical pre-formulation ESAM (aqueous emulsion of ethanolic extract from \u003cem\u003eAnnona mucosa\u003c/em\u003e seeds) and Anosom\u003csup\u003e®\u003c/sup\u003e (acetogenin annonin) \u003cstrong\u003e(b). \u003c/strong\u003e\u003csup\u003ea,b\u003c/sup\u003eLC\u003csub\u003e90\u003c/sub\u003e values from Ansante et al. (2015, 2017) and confirmed in this study\u003c/p\u003e","description":"","filename":"floatimage1.png","url":"https://assets-eu.researchsquare.com/files/rs-5823057/v1/2567317d7ff6359fe8cfe10e.png"},{"id":74551814,"identity":"7e5e5d7c-f5f0-42e1-a840-a973ecf813c9","added_by":"auto","created_at":"2025-01-23 11:00:18","extension":"png","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":137400,"visible":true,"origin":"","legend":"\u003cp\u003eMean mortality (± SE) of \u003cem\u003eD. luteipes\u003c/em\u003e developmental stages exposed to synthetic and botanical insecticides 48h after exposure. Different letters within each stage indicate significant differences (Tukey, \u003cem\u003ep \u003c/em\u003e\u0026lt; 0.05). EFAMON (aqueous emulsion of the methanolic fraction of the ethanolic extract of \u003cem\u003eAnnona montana\u003c/em\u003e leaves); ESAM (aqueous emulsion of the ethanolic extract of \u003cem\u003eAnnona mucosa\u003c/em\u003e seeds); Anosom\u003csup\u003e®\u003c/sup\u003e (acetogenin annonin); Azamax\u003csup\u003e®\u003c/sup\u003e (azadirachtin + 3-tigloylazadirachtol); Premio\u003csup\u003e®\u003c/sup\u003e (chlorantraniliprole)\u003c/p\u003e","description":"","filename":"floatimage2.png","url":"https://assets-eu.researchsquare.com/files/rs-5823057/v1/f24f741f77ddaa6c46e51434.png"},{"id":74550885,"identity":"01760d47-dc92-45a0-b8a9-f0f038911c00","added_by":"auto","created_at":"2025-01-23 10:52:18","extension":"png","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":86195,"visible":true,"origin":"","legend":"\u003cp\u003ePredation capacity (%) ± SE of \u003cem\u003eDoru luteipes\u003c/em\u003e adult on \u003cem\u003eS. frugiperda\u003c/em\u003e larvae (1st instar) after exposure to synthetic and botanical insecticides. Different letters among treatments indicate significant differences (Tukey, \u003cem\u003ep\u003c/em\u003e \u0026lt; 0.05; ± SE). EFAMON (aqueous emulsion of the methanolic fraction of the ethanolic extract of \u003cem\u003eAnnona montana\u003c/em\u003e leaves); ESAM (aqueous emulsion of the ethanolic extract of \u003cem\u003eAnnona mucosa\u003c/em\u003e seeds); Anosom\u003csup\u003e®\u003c/sup\u003e (acetogenin annonin); Azamax\u003csup\u003e®\u003c/sup\u003e (azadirachtin + 3-tigloylazadirachtol); Premio\u003csup\u003e®\u003c/sup\u003e (chlorantraniliprole)\u003c/p\u003e","description":"","filename":"floatimage3.png","url":"https://assets-eu.researchsquare.com/files/rs-5823057/v1/138007a79fdd0499b6e02a38.png"},{"id":74550889,"identity":"749b9072-4672-4244-a8de-8c3d8c7147fe","added_by":"auto","created_at":"2025-01-23 10:52:18","extension":"png","order_by":4,"title":"Figure 4","display":"","copyAsset":false,"role":"figure","size":189888,"visible":true,"origin":"","legend":"\u003cp\u003eMeans (± SE) of velocity \u003cstrong\u003e(a)\u003c/strong\u003e and distance moved \u003cstrong\u003e(b)\u003c/strong\u003e traveled by adult \u003cem\u003eD. luteipes\u003c/em\u003e exposed to synthetic and botanical insecticides. Different letters among treatments indicate significant differences (Tukey, \u003cem\u003ep\u003c/em\u003e \u0026lt; 0.05). EFAMON (aqueous emulsion of the methanolic fraction of the ethanolic extract of \u003cem\u003eAnnona montana\u003c/em\u003e leaves); ESAM (aqueous emulsion of the ethanolic extract of \u003cem\u003eAnnona mucosa\u003c/em\u003e seeds); Anosom\u003csup\u003e®\u003c/sup\u003e (acetogenin annonin); Azamax\u003csup\u003e®\u003c/sup\u003e (azadirachtin + 3-tigloylazadirachtol); Premio\u003csup\u003e®\u003c/sup\u003e (chlorantraniliprole)\u003c/p\u003e","description":"","filename":"floatimage4.png","url":"https://assets-eu.researchsquare.com/files/rs-5823057/v1/0a5c9d89a1927bbd383388f3.png"},{"id":74553387,"identity":"3a04d656-6f66-4eaa-a3a3-151b51c8e6bb","added_by":"auto","created_at":"2025-01-23 11:16:22","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":1841021,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-5823057/v1/18fac9f1-a836-4856-bc26-615975b28da0.pdf"}],"financialInterests":"","formattedTitle":"Investigating the selectivity of botanical and synthetic insecticides on Doru luteipes: there is no simple answer","fulltext":[{"header":"Introduction","content":"\u003cp\u003eCombining chemical and biological control is a key precept in Integrated Pest Management (IPM) programs, and selectivity studies provide essential information for this achievement. In this context, a selective compound should effectively control the target pest while minimizing adverse effects on natural enemies (Castle and Naranjo \u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e2009\u003c/span\u003e; Gentz et al. \u003cspan citationid=\"CR31\" class=\"CitationRef\"\u003e2010\u003c/span\u003e; Bueno et al. \u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; Torres and Bueno \u003cspan citationid=\"CR86\" class=\"CitationRef\"\u003e2018\u003c/span\u003e; Serr\u0026atilde;o et al. \u003cspan citationid=\"CR75\" class=\"CitationRef\"\u003e2022\u003c/span\u003e). Recent efforts have focused on ensuring that newly introduced insecticide molecules are environmentally friendly, promoting a better agroecosystem balance. Examples of these new molecules include botanical insecticides, considered promising alternatives for pest management and less harmful to non-target organisms, along with organosynthetic compounds such as diamides (Ishaaya et al. \u003cspan citationid=\"CR41\" class=\"CitationRef\"\u003e2007\u003c/span\u003e; Turchen et al. \u003cspan citationid=\"CR87\" class=\"CitationRef\"\u003e2014\u003c/span\u003e; Gontijo et al. \u003cspan citationid=\"CR35\" class=\"CitationRef\"\u003e2015\u003c/span\u003e; Ndakidemi et al. \u003cspan citationid=\"CR62\" class=\"CitationRef\"\u003e2016\u003c/span\u003e; Bernardi et al. \u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; Rezende-Teixeira et al. \u003cspan citationid=\"CR69\" class=\"CitationRef\"\u003e2022\u003c/span\u003e; Sparks and Bryant \u003cspan citationid=\"CR82\" class=\"CitationRef\"\u003e2022\u003c/span\u003e; Cong et al. \u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e2023\u003c/span\u003e; Schmidt-Jeffris \u003cspan citationid=\"CR74\" class=\"CitationRef\"\u003e2023\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eThe fall armyworm, \u003cem\u003eSpodoptera frugiperda\u003c/em\u003e (J.E. Smith) (Lepidoptera: Noctuidae), is a significant agricultural pest that affects economically important crops, such as corn, cotton, soybean, rice, and wheat. Control efforts have been challenged by resistance to various chemical groups and \u003cem\u003eBt\u003c/em\u003e corn, which has intensified the search for new management alternatives (Montezano et al. \u003cspan citationid=\"CR53\" class=\"CitationRef\"\u003e2018\u003c/span\u003e; Tay et al. \u003cspan citationid=\"CR84\" class=\"CitationRef\"\u003e2023\u003c/span\u003e; Mota-Sanchez and Wise \u003cspan citationid=\"CR57\" class=\"CitationRef\"\u003e2024\u003c/span\u003e). Among the promising options are botanical insecticides, such as extracts from \u003cem\u003eAnnona mucosa\u003c/em\u003e and \u003cem\u003eAnnona montana\u003c/em\u003e plants, and the commercial botanical insecticide Anosom\u0026reg;, derived from \u003cem\u003eAnnona squamosa\u003c/em\u003e plant. These compounds are rich in acetogenins, a class of natural products consisting of long-chain fatty acids with a 2-propanol unit, and they exhibit distinct modes of action (Colom et al. \u003cspan citationid=\"CR19\" class=\"CitationRef\"\u003e2009\u003c/span\u003e; Di Toto Blessing et al. \u003cspan citationid=\"CR26\" class=\"CitationRef\"\u003e2012\u003c/span\u003e; Ansante et al. \u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e2015\u003c/span\u003e, \u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; Costa et al. \u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e2016\u003c/span\u003e; Hidalgoa et al. \u003cspan citationid=\"CR40\" class=\"CitationRef\"\u003e2020\u003c/span\u003e). Other registered compounds for controlling \u003cem\u003eS. frugiperda\u003c/em\u003e include the commercial botanical insecticide Azamax\u0026reg;, which is based on azadirachtin and 3-tigloylazadiractol from the \u003cem\u003eAzadirachta indica\u003c/em\u003e plant, and the commercial organosynthetic insecticide Premio\u0026reg;, whose active ingredient is chlorantraniliprole, belonging to the diamide group (MAPA, \u003cspan citationid=\"CR52\" class=\"CitationRef\"\u003e2024\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eEffective management of \u003cem\u003eS. frugiperda\u003c/em\u003e requires that the use of chemical insecticides be compatible with the natural enemies involved in biological control, such as the predator \u003cem\u003eDoru luteipes\u003c/em\u003e (Scudder) (Dermaptera: Forficulidae). This predator is commonly found in corn crops, feeding on eggs and larvae of \u003cem\u003eS. frugiperda\u003c/em\u003e. Nymphs of \u003cem\u003eD. luteipes\u003c/em\u003e can consume up to 10 eggs or larvae per day, while adults can consume up to 20 first- and second-instar larvae (Cruz et al. \u003cspan citationid=\"CR23\" class=\"CitationRef\"\u003e1995\u003c/span\u003e; Cruz \u003cspan citationid=\"CR22\" class=\"CitationRef\"\u003e2007\u003c/span\u003e; Pasini et al. \u003cspan citationid=\"CR66\" class=\"CitationRef\"\u003e2010\u003c/span\u003e; Pacheco \u003cspan citationid=\"CR64\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). Additionally, as a polyphagous predator, \u003cem\u003eD. luteipes\u003c/em\u003e is capable of preying on other agriculturally significant pests (Romero Sueldo and Virila \u003cspan citationid=\"CR71\" class=\"CitationRef\"\u003e2009\u003c/span\u003e; Romero Sueldo et al. \u003cspan citationid=\"CR72\" class=\"CitationRef\"\u003e2014\u003c/span\u003e; Silva et al. \u003cspan citationid=\"CR78\" class=\"CitationRef\"\u003e2023\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eHowever, achieving compatibility between chemical insecticides and natural enemies can be challenging. Selectivity depends on several factors, including the product's physicochemical composition, the target species, the method of exposure, the insect's developmental stages, its behavior, and its detoxification mechanisms (Godoy et al. \u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e2010\u003c/span\u003e; He et al. \u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e2019\u003c/span\u003e; V\u0026aacute;zquez \u003cspan citationid=\"CR88\" class=\"CitationRef\"\u003e2019\u003c/span\u003e; Silva et al. \u003cspan citationid=\"CR77\" class=\"CitationRef\"\u003e2020\u003c/span\u003e; Potin et al. \u003cspan citationid=\"CR67\" class=\"CitationRef\"\u003e2022\u003c/span\u003e). Although most of the insecticides mentioned earlier for controlling \u003cem\u003eS. frugiperda\u003c/em\u003e are derived from botanical sources, and the organosynthetic insecticide (chlorantraniliprole) is reported to be selective towards non-target organisms, ecotoxicology studies need to be conducted considering the specific characteristics of the pest, the insecticide, the natural enemy, and the exposure method (Gontijo et al. \u003cspan citationid=\"CR35\" class=\"CitationRef\"\u003e2015\u003c/span\u003e; Haddi et al. \u003cspan citationid=\"CR38\" class=\"CitationRef\"\u003e2020\u003c/span\u003e; Serr\u0026atilde;o et al. \u003cspan citationid=\"CR75\" class=\"CitationRef\"\u003e2022\u003c/span\u003e; Arroyo et al. \u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e2023\u003c/span\u003e). Moreover, these studies should assess not only direct lethal effects but also sublethal effects, which may compromise the effectiveness of natural enemies and the sustainability of agricultural system (Haddi et al. \u003cspan citationid=\"CR38\" class=\"CitationRef\"\u003e2020\u003c/span\u003e).(Desneux et al. \u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e2007\u003c/span\u003e; M\u0026uuml;ller \u003cspan citationid=\"CR58\" class=\"CitationRef\"\u003e2018\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eGiven that both synthetic and botanical insecticides, as well as biological control utilizing \u003cem\u003eD. luteipes\u003c/em\u003e, are considered essential tools for \u003cem\u003eS. frugiperda\u003c/em\u003e management in food production systems, this study tested the following hypotheses: (I) residues of botanical and synthetic insecticides may impact \u003cem\u003eD. luteipes\u003c/em\u003e differentially across its life stages, (II) affect its behavior, and (III) cause transgenerational effects. Identifying selective products is fundamental to advancing the integrated management of \u003cem\u003eS. frugiperda\u003c/em\u003e while safeguarding \u003cem\u003eD. luteipes.\u003c/em\u003e\u003c/p\u003e"},{"header":"Materials and methods","content":"\u003cdiv id=\"Sec3\" class=\"Section2\"\u003e \u003ch2\u003eInsect rearing\u003c/h2\u003e \u003cp\u003eAdults of \u003cem\u003eD. luteipes\u003c/em\u003e were collected from corn crops without insecticide application in an experimental field in Piracicaba, S\u0026atilde;o Paulo, Brazil (22\u0026deg;42'49.1\"S 47\u0026deg;37'32.8\"W). Plastic containers (25.5 cm long \u0026times; 18.5 cm wide \u0026times; 8 cm high) covered with organza fabric and brown paper were used for laboratory maintenance. Inside the containers, accordion paper was provided as a refuge and shelter. Both adults and nymphs were fed ad libitum with an artificial diet developed by Guimar\u0026atilde;es et al. (\u003cspan citationid=\"CR37\" class=\"CitationRef\"\u003e2006\u003c/span\u003e), consisting of cat food (35%), wheat germ (27%), brewer's yeast (23%), powdered milk (14%), Nipagin (0.5%), and ascorbic acid (0.5%). Plastic straws (0.8 cm diameter) containing moistened cotton were used as substrates for oviposition (Naranjo-Guevara et al. \u003cspan citationid=\"CR60\" class=\"CitationRef\"\u003e2017\u003c/span\u003e). As this species exhibits parental care, females were transferred with their respective eggs to new containers after oviposition. They remained there for fourteen days before being reintegrated into the colony. The nymphs were kept separate until adult emergence, with some used in experiments and others reserved for colony maintenance. The insects used in the bioassays belonged to the 14th laboratory-reared generations.\u003c/p\u003e \u003cp\u003e \u003cem\u003eSpodoptera frugiperda\u003c/em\u003e larvae were obtained from a susceptible population maintained in the laboratory for over 20 years. The pupae and adults were kept in cages made of PVC tubes (20 cm in diameter \u0026times; 20 cm in height), internally lined with white paper to facilitate oviposition. Neonate larvae were reared in 100 mL plastic cups containing an artificial diet (Greene et al. \u003cspan citationid=\"CR36\" class=\"CitationRef\"\u003e1976\u003c/span\u003e). Upon reaching the third instar, they were individualized and kept until the pupal stage, at this point, they were transferred back to the cages. Adults were fed a 10% honey solution. All insect rearing and experiments were conducted in a climate-controlled room (temperature: 25\u0026thinsp;\u0026plusmn;\u0026thinsp;1\u0026deg;C, relative humidity: 60\u0026thinsp;\u0026plusmn;\u0026thinsp;10%, and photoperiod: 12 L:12 D).\u003c/p\u003e \u003c/div\u003e\n\u003ch3\u003eObtaining the treatments\u003c/h3\u003e\n\u003cp\u003eThe treatments involved two non-commercial botanical pre-formulations and three commercial insecticides, which consisted of two botanical and one organosynthetic. The pre-formulations included (1) an aqueous emulsion of the methanolic fraction from the ethanolic extract of \u003cem\u003eAnnona montana\u003c/em\u003e leaves (EFAMON) and (2) an aqueous emulsion of the ethanolic extract from \u003cem\u003eAnnona mucosa\u003c/em\u003e seeds (ESAM). The commercial insecticides comprised (1) Anosom\u0026reg; 1 EC, a botanical product based on acetogenins (annonin) (AgriLife SOM Phytopharma Ltda., Hyderabad, India); (2) Azamax\u0026reg; 1.2 EC, also a botanical insecticide containing limonoids (azadirachtin and 3-tigloylazadirachtol) (UPL Brasil Ltda., Campinas, S\u0026atilde;o Paulo, Brazil); and (3) Premio\u0026reg; 200 SC, an organosynthetic insecticide with chlorantraniliprole as the active ingredient (FMC Qu\u0026iacute;mica do Brasil Ltda., Campinas, S\u0026atilde;o Paulo, Brazil). Distilled water and the solvents used in the pre-formulations were the control group.\u003c/p\u003e\n\u003ch3\u003ePreparation of botanical pre-formulations\u003c/h3\u003e\n\u003cp\u003eBotanical pre-formulations were prepared using ethanolic extracts from \u003cem\u003eA. montana\u003c/em\u003e leaves and \u003cem\u003eA. mucosa\u003c/em\u003e seeds. The leaves and seeds were dried in an oven at 38\u0026deg;C for 48h, ground in a knife mill, and the resulting powder was extracted with ethanol. After three days of rest, the material was filtered, and the solvent was removed in a rotary evaporator at 50\u0026deg;C and \u0026minus;\u0026thinsp;600 mmHg. The \u003cem\u003eA. montana\u003c/em\u003e extract was then subjected to liquid-liquid partition to separate phases with different chemical affinities and obtain the methanolic fraction, according to the procedure described by Lima et al. (\u003cspan citationid=\"CR47\" class=\"CitationRef\"\u003e2022\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eEmulsions of the methanolic fraction of \u003cem\u003eA. montana\u003c/em\u003e and the ethanolic extract of \u003cem\u003eA. mucosa\u003c/em\u003e were prepared by adding the surfactants Triton\u0026reg; X-100 (0.1%, v v\u003csup\u003e\u0026minus;\u0026thinsp;1\u003c/sup\u003e) and Tween\u0026reg; 80 (1%, v v\u003csup\u003e\u0026minus;\u0026thinsp;1\u003c/sup\u003e), along with a mixture (1%, v v\u003csup\u003e\u0026minus;\u0026thinsp;1\u003c/sup\u003e) of acetone and methanol (1:1, v v\u003csup\u003e\u0026minus;\u0026thinsp;1\u003c/sup\u003e). These components helped to break the surface tension of the water, improve leaf adhesion, and facilitate the dilution of the emulsions.\u003c/p\u003e \u003cp\u003e \u003cb\u003eLethal concentration (LC) of\u003c/b\u003e \u003cb\u003eS. frugiperda\u003c/b\u003e\u003c/p\u003e \u003cp\u003eConcentration-response curves were performed to determine the lethal concentration of treatments required to kill the pest \u003cem\u003eS. frugiperda\u003c/em\u003e. Different treatment concentrations (at least eight) were incorporated into 100 g of artificial diet. After preparation, 1 mL of the contaminated diet was distributed into wells of 128-cell plastic plates (Advento do Brasil, S\u0026atilde;o Paulo, Brazil) using a hypodermic syringe (BD PlastipaK\u0026trade;). The plates were infested with neonate larvae (\u0026lt;\u0026thinsp;24 hours old) and sealed with transparent plastic lids for aeration. Mortality was assessed daily over seven days. For the EFAMON treatment, the concentrations, before being added to the diet, were pre-diluted in 6 mL of acetone and methanol (1:1, v/v). These same solvents were used in the control treatment. A completely randomized design was adopted, with four replicates per treatment and 16 insects per replicate. For the ESAM and Anosom\u0026reg;, as their concentration-response curves (LC) for \u003cem\u003eS. frugiperda\u003c/em\u003e had already been determined in previous studies a mortality bioassay was conducted to confirm these values (ESAM LC\u003csub\u003e90\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;1,386.0 mg kg\u003csup\u003e\u0026minus;\u0026thinsp;1\u003c/sup\u003e; Anosom\u0026reg; LC\u003csub\u003e90\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;2,959.0 mg kg\u003csup\u003e\u0026minus;\u0026thinsp;1\u003c/sup\u003e) (Ansante et al. \u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e2015\u003c/span\u003e, \u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e2017\u003c/span\u003e). The bioassay followed the same procedures described above, confirming the toxicity of these two treatments against the pest.\u003c/p\u003e \u003cp\u003e \u003cb\u003eSelectivity bioassays on\u003c/b\u003e \u003cb\u003eDoru luteipes\u003c/b\u003e\u003c/p\u003e \u003cp\u003eSelectivity bioassays were conducted to assess the lethal and sublethal effects of treatments on \u003cem\u003eDoru luteipes\u003c/em\u003e. The predator was exposed to tarsal contact with leaves treated with the lethal concentration (LC\u003csub\u003e90\u003c/sub\u003e) previously determined for the pest. All experiments were performed in a completely randomized design and maintained in a climate-controlled room (temperature: 25\u0026thinsp;\u0026plusmn;\u0026thinsp;1\u0026deg;C, relative humidity: 60\u0026thinsp;\u0026plusmn;\u0026thinsp;10%, and a photoperiod of 12 L: 12 D h).\u003c/p\u003e\n\u003ch3\u003eLethal effect on developmental stages\u003c/h3\u003e\n\u003cp\u003eTo evaluate the lethal effect of treatments on \u003cem\u003eD. luteipes\u003c/em\u003e mortality, corn leaf discs (vegetative stage, V5) with 4.5 cm diameter were cut and dipped in the treatment solutions for 10 seconds. Distilled water and the solvents from pre-formulations were used as a control. After drying, the discs were placed in plastic containers (4.5 cm diameter and 5.0 cm height) containing carrageenan (2.5%, w v\u003csup\u003e\u0026minus;\u0026thinsp;1\u003c/sup\u003e) at the base to maintain moisture. Subsequently, insects were grouped by developmental stage (1st, 2nd, 3rd, 4th instars, and adults), all 24 hours old, and placed in containers containing treated leaves to allow tarsal contact with the treatments. An artificial diet was provided for feeding, along with moistened cotton to maintain adequate humidity. The containers were sealed with perforated lids to allow aeration, and mortality was recorded 48 hours after exposure. Each treatment consisted of five replicates, with six insects per replicate (three males and three females for the adult stage).\u003c/p\u003e\n\u003ch3\u003eSublethal effects\u003c/h3\u003e\n\u003cdiv id=\"Sec8\" class=\"Section2\"\u003e \u003ch2\u003ePredation and walking behavior\u003c/h2\u003e \u003cp\u003eFor the sublethal effects assessment, adult \u003cem\u003eD. luteipes\u003c/em\u003e were exposed to the LC\u003csub\u003e90\u003c/sub\u003e concentration of the treatments for 24 hours, following the same procedure described previously. This concentration was chosen because no significant mortality was observed in adults during the lethal effect bioassay.\u003c/p\u003e \u003cp\u003eAfter exposure, to evaluate predation, each insect was individually transferred to a plastic container (4.5 cm in diameter \u0026times; 6.5 cm in height) and provided with 20 first-instar larvae of \u003cem\u003eSpodoptera frugiperda\u003c/em\u003e. After 12 hours, the number of preyed larvae was recorded. The experiment included six treatments, ten replicates per treatment, consisting of five males and five females, with one insect per replicate, meaning one adult for every 20 larvae of \u003cem\u003eS. frugiperda\u003c/em\u003e. All adults used in the experiment were no more than 24 hours old and had not received any artificial diet before the test.\u003c/p\u003e \u003cp\u003eThe behavioral bioassay aimed to assess whether the treatments affected the movement activity of the insects. Each experimental unit consisted of four adult insects kept in plastic containers (25.5 cm length \u0026times; 18.5 cm width \u0026times; 8 cm height). After the exposure period (24h), each replicate was filmed for 10 minutes using a Sony Handycam camcorder (Hdr-cx405 Full Hd) positioned perpendicular to the insect container. The ambient light was covered with red cellophane. A total of six replicates per treatment were performed. Movement data were analyzed using an automated image capture system (EthoVision, Noldus et al. \u003cspan citationid=\"CR63\" class=\"CitationRef\"\u003e2001\u003c/span\u003e). The variables analyzed were \u0026ldquo;Distance moved\u0026rdquo; (cm) and \u0026ldquo;Velocity\u0026rdquo; (cm s\u003csup\u003e\u0026minus;\u0026thinsp;1\u003c/sup\u003e). \u0026ldquo;Distance moved\u0026rdquo; was defined as the distance traveled by the subject's center of mass from the previous to the current sample. \u0026ldquo;Velocity\u0026rdquo; was defined as the distance traveled by the subject's center of mass per unit time (Cann et al. \u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e2013\u003c/span\u003e). Both experiments were conducted at night (from 7 pm to 9 pm) when \u003cem\u003eD. luteipes\u003c/em\u003e exhibits increased predatory activity (Naranjo-Guevara et al. \u003cspan citationid=\"CR60\" class=\"CitationRef\"\u003e2017\u003c/span\u003e).\u003c/p\u003e \u003c/div\u003e\n\u003ch3\u003eBiological parameters and transgenerational effects\u003c/h3\u003e\n\u003cp\u003eTo evaluate the sublethal effects of treatments on the biological parameters of \u003cem\u003eD. luteipes\u003c/em\u003e, newly emerged adults (less than 24 hours old) were exposed to treated leaves for 24 hours. After exposure, ten couples/treatment were formed and placed individually in containers containing an artificial diet and moistened cotton. Daily observations recorded longevity and reproductive parameters, including the pre-oviposition period and fecundity. Once the females laid their eggs, the males were separated until the nymphs hatched, as \u003cem\u003eD. luteipes\u003c/em\u003e exhibit parental care, and the presence of males could stress females during this period.\u003c/p\u003e \u003cp\u003eFrom these couples, 10 egg masses (30 eggs per mass) were selected to assess the development, viability, and sex ratio of the F\u003csub\u003e1\u003c/sub\u003e generation. The number of males and females was determined by differentiating the cerci: more curved cerci indicate males, while straight cerci indicate females. Subsequently, a fertility life table was constructed to investigate the effects of the treatment on the population growth. Biological data were collected, including \u003cem\u003ex\u003c/em\u003e\u0026thinsp;=\u0026thinsp;average age of insects from egg stage, \u003cem\u003elx\u003c/em\u003e\u0026thinsp;=\u0026thinsp;survival rate, \u003cem\u003emx\u003c/em\u003e\u0026thinsp;=\u0026thinsp;specific fertility, and \u003cem\u003elx.mx\u003c/em\u003e\u0026thinsp;=\u0026thinsp;total number of females born at age \u003cem\u003ex\u003c/em\u003e. These data were used to estimate the life table parameters: net reproductive rate (\u003cem\u003eR\u003c/em\u003e\u003csub\u003e\u003cem\u003e0\u003c/em\u003e\u003c/sub\u003e), mean generation time (\u003cem\u003eT\u003c/em\u003e), intrinsic rate of increase (\u003cem\u003er\u003c/em\u003e\u003csub\u003e\u003cem\u003em\u003c/em\u003e\u003c/sub\u003e), and finite rate of population increase (\u003cem\u003eλ\u003c/em\u003e) (Maia et al. \u003cspan citationid=\"CR51\" class=\"CitationRef\"\u003e2014\u003c/span\u003e). The experiment included six treatments, each with 10 replicates (one pair per replicate). Ten egg masses/couples containing 30 eggs each were used to assess egg cohorts.\u003c/p\u003e\n\u003ch3\u003eStatistical analyses\u003c/h3\u003e\n\u003cp\u003eThe mortality data of developmental stages and predation capacity were analyzed by fitting a Generalized Linear Model (GLM) assuming binomial distribution. Behavior data were analyzed by fitting GLM with Gaussian distribution. In contrast, longevity, pre-oviposition period, fecundity, F\u003csub\u003e1\u003c/sub\u003e generation development, viability, and sexual ratio data were analyzed using GLM with Poisson distribution, with correction for overdispersion when necessary. For all models, the fit quality was assessed using a half-normal plot with simulated envelopes at the 95% level (Moral et al. \u003cspan citationid=\"CR55\" class=\"CitationRef\"\u003e2017\u003c/span\u003e). The fertility life table was constructed using the lifetable.R procedure described by Maia et al. (\u003cspan citationid=\"CR51\" class=\"CitationRef\"\u003e2014\u003c/span\u003e) using the Jackknife method, and parameters were analyzed using GLM with Gaussian distribution. For all fitted models, the deviance analysis was conducted, and when necessary, means were compared using Tukey's test (\u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.05). All analyses were performed using R statistical software version 4.2.1 (R Core Team, \u003cspan citationid=\"CR68\" class=\"CitationRef\"\u003e2021\u003c/span\u003e; \u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003ehttp://www.R-project.org\u003c/span\u003e\u003cspan address=\"http://www.R-project.org\" targettype=\"URL\" class=\"RefTarget\"\u003e\u003c/span\u003e\u003c/span\u003e).\u003c/p\u003e"},{"header":"Results","content":"\u003cp\u003e \u003cb\u003eLethal concentration (LC) of\u003c/b\u003e \u003cb\u003eS. frugiperda\u003c/b\u003e\u003c/p\u003e \u003cp\u003eThe lethal concentration (LC) required for the non-commercial botanical pre-formulation EFAMON to cause 90% mortality in \u003cem\u003eSpodoptera frugiperda\u003c/em\u003e larvae was 10,949.05 mg kg⁻\u0026sup1; (Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e, Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003ea). Among the commercial insecticides, the botanical product Azamax\u0026reg; (azadirachtin\u0026thinsp;+\u0026thinsp;3-tigloylazadirachtol) showed an LC\u003csub\u003e90\u003c/sub\u003e of 65.429 mg kg⁻\u0026sup1;, while the synthetic insecticide Premio\u0026reg; (chlorantraniliprole) exhibited the lowest LC\u003csub\u003e90\u003c/sub\u003e value, 0.433 mg kg⁻\u0026sup1; (Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e, Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003ea). The toxicity bioassay confirmed that the lethal concentrations of the botanical pre-formulation ESAM (LC\u003csub\u003e90\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;1,386.0 mg kg⁻\u0026sup1;) and the botanical insecticide Anosom\u0026reg; (LC\u003csub\u003e90\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;2,959.0 mg kg⁻\u0026sup1;) effectively caused 90% mortality in the pest population (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003eb).\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab1\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 1\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eLethal concentrations (LC\u003csub\u003e50\u003c/sub\u003e and LC\u003csub\u003e90\u003c/sub\u003e) of botanical and synthetic insecticides for \u003cem\u003eSpodoptera frugiperda\u003c/em\u003e larvae seven days after exposure\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"7\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\"\u0026plusmn;\" class=\"colspec\" colname=\"c5\" colnum=\"5\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c6\" colnum=\"6\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c7\" colnum=\"7\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e \u003cp\u003eTreatments\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003e\u003cem\u003eN\u003c/em\u003e\u003csup\u003e\u003cem\u003eb\u003c/em\u003e\u003c/sup\u003e\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c3\"\u003e \u003cp\u003eLC\u003csub\u003e50\u003c/sub\u003e\u003c/p\u003e \u003cp\u003e(mg kg\u003csup\u003e\u0026minus;\u0026thinsp;1\u003c/sup\u003e) (95% CI\u003csup\u003ec\u003c/sup\u003e)\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c4\"\u003e \u003cp\u003eLC\u003csub\u003e90\u003c/sub\u003e\u003c/p\u003e \u003cp\u003e(95% CI)\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c5\"\u003e \u003cp\u003eSlope\u0026thinsp;\u0026plusmn;\u0026thinsp;SE\u003csup\u003ed\u003c/sup\u003e\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c6\"\u003e \u003cp\u003e\u003cem\u003eχ\u003c/em\u003e\u003csup\u003e\u003cem\u003e2\u003c/em\u003e\u003c/sup\u003e\u003c/p\u003e \u003cp\u003e\u003cem\u003e(df\u003c/em\u003e \u003csup\u003e\u003cem\u003ee\u003c/em\u003e\u003c/sup\u003e\u003cem\u003e)\u003c/em\u003e\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c7\"\u003e \u003cp\u003e\u003cem\u003eP\u003c/em\u003e\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003ePre-formulation\u003c/p\u003e \u003cp\u003eEFAMON\u003csup\u003ea\u003c/sup\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e452\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e2,440.70\u003c/p\u003e \u003cp\u003e(1.960,76-3.038,12)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e10,949.05\u003c/p\u003e \u003cp\u003e(8,115.53-14,771,89)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\"\u0026plusmn;\" colname=\"c5\"\u003e \u003cp\u003e1.93\u0026thinsp;\u0026plusmn;\u0026thinsp;0.20\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e9.39 (5)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c7\"\u003e \u003cp\u003e0.094\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eAzamax\u0026reg; EC, 1.2g a.i L\u003csup\u003e\u0026minus;\u0026thinsp;1\u003c/sup\u003e\u003c/p\u003e \u003cp\u003e(Azadirachtin\u0026thinsp;+\u0026thinsp;3-tigloylazadirachtol)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e442\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e10.619\u003c/p\u003e \u003cp\u003e(8.668\u0026ndash;13.010)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e65.429\u003c/p\u003e \u003cp\u003e(44.279\u0026ndash;96.680)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\"\u0026plusmn;\" colname=\"c5\"\u003e \u003cp\u003e1.62\u0026thinsp;\u0026plusmn;\u0026thinsp;0.16\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e8.04 (4)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c7\"\u003e \u003cp\u003e0.090\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003ePremio\u0026reg; SC, 200g a.i. L\u003csup\u003e\u0026minus;\u0026thinsp;1\u003c/sup\u003e\u003c/p\u003e \u003cp\u003e(Chlorantraniliprole)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e523\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e0.176\u003c/p\u003e \u003cp\u003e(0.154\u0026ndash;0.201)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e0.433\u003c/p\u003e \u003cp\u003e(0.371\u0026ndash;0.506)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\"\u0026plusmn;\" colname=\"c5\"\u003e \u003cp\u003e3.28\u0026thinsp;\u0026plusmn;\u0026thinsp;0.28\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e2.58 (4)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c7\"\u003e \u003cp\u003e0.630\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003ctfoot\u003e \u003ctr\u003e\u003ctd colspan=\"7\"\u003e\u003csup\u003ea\u003c/sup\u003eEFAMON = Aqueous emulsion of the methanolic fraction of the ethanolic extract of \u003cem\u003eAnnona montana\u003c/em\u003e leaves. \u003csup\u003eb\u003c/sup\u003e\u003cem\u003eN\u003c/em\u003e = Number of tested \u003cem\u003eS. frugiperda\u003c/em\u003e. \u003csup\u003ec\u003c/sup\u003eCI = Confidence Interval at 95% error probability. \u003csup\u003ed\u003c/sup\u003eSE = Standard Error. \u003csup\u003ee\u003c/sup\u003e\u003cem\u003edf\u003c/em\u003e = Degrees of freedom\u003c/td\u003e\u003c/tr\u003e \u003c/tfoot\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cdiv id=\"Sec12\" class=\"Section2\"\u003e \u003ch2\u003eLethal effect on developmental stages\u003c/h2\u003e \u003cp\u003eThe treatments affected the survival of \u003cem\u003eD. luteipes\u003c/em\u003e at all nymphal stages (χ\u0026sup2;= 46.633, df\u0026thinsp;=\u0026thinsp;20;120, \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.001) (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003e). Premio\u0026reg; (chlorantraniliprole) caused the highest mortality, with values above 90% in the first instar and over 50% in other instars. However, this effect did not differ from that of ESAM (aqueous emulsion of the ethanolic extract of \u003cem\u003eAnnona mucosa\u003c/em\u003e seeds) and Anosom\u0026reg; (acetogenin annonin\u003cem\u003e)\u003c/em\u003e in the first instar. For nymphs in the 2nd to 4th instars, botanical insecticides resulted in mortality below 30%. The tested treatments did not significantly affect mortality in the adult stage (F\u0026thinsp;=\u0026thinsp;1.547, df\u0026thinsp;=\u0026thinsp;5;120, p\u0026thinsp;=\u0026thinsp;0.1804) (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003e).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec13\" class=\"Section2\"\u003e \u003ch2\u003ePredation and walking behavior\u003c/h2\u003e \u003cp\u003eThe interaction between the sex of adults and treatments was not significant (F\u0026thinsp;=\u0026thinsp;0.988, df\u0026thinsp;=\u0026thinsp;5;48, \u003cem\u003ep\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.435); however, the average predation capacity of males was higher than that of females (F\u0026thinsp;=\u0026thinsp;16.536, df\u0026thinsp;=\u0026thinsp;1;48, \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.001), with males preying on 89% and females on 77% of the prey offered. Regarding the treatments, there were differences in the predation of \u003cem\u003eS. frugiperda\u003c/em\u003e by \u003cem\u003eD. luteipes\u003c/em\u003e (F\u0026thinsp;=\u0026thinsp;33.967, df\u0026thinsp;=\u0026thinsp;5;48, \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.001), with adults exposed to leaves treated with the insecticide Premio\u0026reg; showing the lowest predation rate (40.5%). In comparison, predation was higher than 86% for other treatments, unlike the control with 92% predation (Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003e).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003eThe walking behavior of adult \u003cem\u003eD. luteipes\u003c/em\u003e was affected by the treatments, with analysis showing effects on velocity (F\u0026thinsp;=\u0026thinsp;4.89, df\u0026thinsp;=\u0026thinsp;5;63, p\u0026thinsp;\u0026lt;\u0026thinsp;0.001) and distance (F\u0026thinsp;=\u0026thinsp;3.506, df\u0026thinsp;=\u0026thinsp;5;63, p\u0026thinsp;\u0026lt;\u0026thinsp;0.01) (Fig.\u0026nbsp;4). A similar pattern was observed for both the \u0026ldquo;Velocity\u0026rdquo; and \u0026ldquo;Distance moved\u0026rdquo; variables, as expected due to the relationship between the variables. The adults contaminated with the synthetic insecticide Premio\u0026reg; exhibited lower locomotor activity, covering shorter distances (433.97 cm) and walking at a slower velocity (0.73 cm s\u003csup\u003e\u0026minus;\u0026thinsp;1\u003c/sup\u003e). However, compared to the other treatments, no significant differences in velocity were found between the synthetic insecticide Premio\u0026reg; (0.73 cm s\u003csup\u003e\u0026minus;\u0026thinsp;1\u003c/sup\u003e) and the commercial botanical insecticide Anosom\u0026reg; (0.98 cm s\u003csup\u003e\u0026minus;\u0026thinsp;1\u003c/sup\u003e) (Fig.\u0026nbsp;4a). No significant differences were observed in the distance moved between Premio\u0026reg; (433.97 cm), Anosom\u0026reg; (570.33 cm), and the negative control group (566.10 cm) (Fig.\u0026nbsp;4b).\u003c/p\u003e \u003cp\u003e \u003cb\u003eFig 4\u003c/b\u003e Means (\u0026plusmn;\u0026thinsp;SE) of velocity \u003cb\u003e(a)\u003c/b\u003e and distance moved \u003cb\u003e(b)\u003c/b\u003e traveled by adult \u003cem\u003eD. luteipes\u003c/em\u003e exposed to synthetic and botanical insecticides. Different letters among treatments indicate significant differences (Tukey, \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.05). EFAMON (aqueous emulsion of the methanolic fraction of the ethanolic extract of \u003cem\u003eAnnona montana\u003c/em\u003e leaves); ESAM (aqueous emulsion of the ethanolic extract of \u003cem\u003eAnnona mucosa\u003c/em\u003e seeds); Anosom\u003csup\u003e\u0026reg;\u003c/sup\u003e (acetogenin annonin); Azamax\u003csup\u003e\u0026reg;\u003c/sup\u003e (azadirachtin\u0026thinsp;+\u0026thinsp;3-tigloylazadirachtol); Premio\u003csup\u003e\u0026reg;\u003c/sup\u003e (chlorantraniliprole)\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec14\" class=\"Section2\"\u003e \u003ch2\u003eInfluence on longevity and reproductive parameters\u003c/h2\u003e \u003cp\u003eAdults exposed to leaves contaminated with the treatments for 24 h showed differences in longevity (Table\u0026nbsp;\u003cspan refid=\"Tab2\" class=\"InternalRef\"\u003e2\u003c/span\u003e). The treatments constituted by ESAM and the synthetic insecticide Premio\u0026reg; reduced adult longevity to 88.88 and 95.17 days, respectively, differing from the control, which was 121.6 days. However, they did not differ from those of the other tested treatments. A similar pattern was observed for males, where Premio\u0026reg; reduced longevity to 71.56 days, differing from the control group, which was 112 days.\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab2\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 2\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eMean longevity (\u0026plusmn;\u0026thinsp;SE) of adult \u003cem\u003eD. luteipes\u003c/em\u003e after exposure to synthetic and botanical insecticides\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"4\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003eTreatments\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colspan=\"3\" nameend=\"c4\" namest=\"c2\"\u003e \u003cp\u003eLongevity (days)\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003eAdult\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c3\"\u003e \u003cp\u003eMale\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c4\"\u003e \u003cp\u003eFemale\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eControl\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e121.6\u0026thinsp;\u0026plusmn;\u0026thinsp;4.75a\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e112.1\u0026thinsp;\u0026plusmn;\u0026thinsp;6.83a\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e133.5\u0026thinsp;\u0026plusmn;\u0026thinsp;3.48a\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eEFAMON\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e115.7\u0026thinsp;\u0026plusmn;\u0026thinsp;5.97ab\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e106.7\u0026thinsp;\u0026plusmn;\u0026thinsp;7.77ab\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e124.7\u0026thinsp;\u0026plusmn;\u0026thinsp;8.22ab\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eESAM\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e88.88\u0026thinsp;\u0026plusmn;\u0026thinsp;6.78c\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e86.90\u0026thinsp;\u0026plusmn;\u0026thinsp;9.47c\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e91.38\u0026thinsp;\u0026plusmn;\u0026thinsp;10.3ab\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eAnosom\u0026reg;\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e105.3\u0026thinsp;\u0026plusmn;\u0026thinsp;4.85abc\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e102.3\u0026thinsp;\u0026plusmn;\u0026thinsp;6.8abc\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e108.4\u0026thinsp;\u0026plusmn;\u0026thinsp;7.16ab\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eAzamax\u0026reg;\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e99.00\u0026thinsp;\u0026plusmn;\u0026thinsp;5.67abc\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e104.1\u0026thinsp;\u0026plusmn;\u0026thinsp;10.16bc\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e93.33\u0026thinsp;\u0026plusmn;\u0026thinsp;4.06ab\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003ePremio\u0026reg;\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e95.17\u0026thinsp;\u0026plusmn;\u0026thinsp;8.50bc\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e71.56\u0026thinsp;\u0026plusmn;\u0026thinsp;7.5abc\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e121.7\u0026thinsp;\u0026plusmn;\u0026thinsp;9.41b\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eF\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e4.00\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e3.34\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e5.15\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003ep\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e\u0026lt;\u0026thinsp;0.01\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e\u0026lt;\u0026thinsp;0.05\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e\u0026lt;\u0026thinsp;0.001\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cp\u003eMeans followed by the same letter in the column do not differ statistically (Tukey, \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.05). EFAMON (aqueous emulsion of the methanolic fraction of the ethanolic extract of \u003cem\u003eAnnona montana\u003c/em\u003e leaves); ESAM (aqueous emulsion of the ethanolic extract of \u003cem\u003eAnnona mucosa\u003c/em\u003e seeds); Anosom\u0026reg; (acetogenin annonin); Azamax\u0026reg; (azadirachtin\u0026thinsp;+\u0026thinsp;3-tigloylazadirachtol); Premio\u0026reg; (chlorantraniliprole)\u003c/p\u003e \u003cp\u003eAmong the reproductive parameters assessed, the pre-oviposition period was influenced by the treatments, with synthetic insecticide Premio\u0026reg; resulting in the shortest pre-oviposition period (9.44 days) compared to the control (13.10 days) and ESAM (13.00 days), indicating rapid sexual maturation of females exposed to this diamide. However, it did not differ statistically from botanical insecticides based on acetogenins (EFAMON and Anosom\u0026reg;) and limonoids (Azamax\u0026reg;). Mean fecundity values ranged from 31.20 to 57.10, with no significant statistical differences observed among the treatments (Table\u0026nbsp;\u003cspan refid=\"Tab3\" class=\"InternalRef\"\u003e3\u003c/span\u003e).\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab3\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 3\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eEffects of synthetic and botanical insecticides on the reproductive parameters of \u003cem\u003eD. luteipes\u003c/em\u003e\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"3\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003eTreatments\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colspan=\"2\" nameend=\"c3\" namest=\"c2\"\u003e \u003cp\u003eReproductive parameters\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003ePre-oviposition (days)\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c3\"\u003e \u003cp\u003eFecundity (eggs/female)\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eControl\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e13.10\u0026thinsp;\u0026plusmn;\u0026thinsp;0.54a\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e53.30\u0026thinsp;\u0026plusmn;\u0026thinsp;8.75a\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eEFAMON\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e12.00\u0026thinsp;\u0026plusmn;\u0026thinsp;0.70ab\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e53.10\u0026thinsp;\u0026plusmn;\u0026thinsp;9.26a\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eESAM\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e13.00\u0026thinsp;\u0026plusmn;\u0026thinsp;1.21a\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e31.20\u0026thinsp;\u0026plusmn;\u0026thinsp;10.37a\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eAnosom\u0026reg;\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e12.44\u0026thinsp;\u0026plusmn;\u0026thinsp;0.80ab\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e39.30\u0026thinsp;\u0026plusmn;\u0026thinsp;7.89a\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eAzamax\u0026reg;\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e11.00\u0026thinsp;\u0026plusmn;\u0026thinsp;0.57ab\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e46.20\u0026thinsp;\u0026plusmn;\u0026thinsp;5.98a\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003ePremio\u0026reg;\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e9.44\u0026thinsp;\u0026plusmn;\u0026thinsp;1.00b\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e57.10\u0026thinsp;\u0026plusmn;\u0026thinsp;9.00a\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eF\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e3.14\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e1.56\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003ep\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e\u0026lt;\u0026thinsp;0.05\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e0.18\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cp\u003eMeans followed (\u0026plusmn;\u0026thinsp;SE) by the same letter in the column do not differ statistically from each other (Tukey \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.05). EFAMON (aqueous emulsion of the methanolic fraction of the ethanolic extract of \u003cem\u003eAnnona montana\u003c/em\u003e leaves); ESAM (aqueous emulsion of the ethanolic extract of \u003cem\u003eAnnona mucosa\u003c/em\u003e seeds); Anosom\u0026reg; (acetogenin annonin); Azamax\u0026reg; (azadirachtin\u0026thinsp;+\u0026thinsp;3-tigloylazadirachtol); Premio\u0026reg; (chlorantraniliprole)\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec15\" class=\"Section2\"\u003e \u003ch2\u003eBiological parameters and transgenerational effects\u003c/h2\u003e \u003cp\u003eThe treatments did not affect the development time and sex ratio of the F\u003csub\u003e1\u003c/sub\u003e generation. The egg incubation and first- and fourth-instar nymph durations were approximately 8 days, while second- and third-instar nymphs lasted about 6 days. The complete cycle, from egg to adult, spanned 36\u0026ndash;37 days, with a balanced sex ratio (close to 0.5) (Table\u0026nbsp;\u003cspan refid=\"Tab4\" class=\"InternalRef\"\u003e4\u003c/span\u003e). However, the viability of fourth-instar nymphs was affected by the treatments. EFAMON resulted in the lowest viability (54.54%), significantly lower than the control (91.91%), Anosom\u0026reg; (93.56%), and Premio\u0026reg; (86.87%) (Table\u0026nbsp;\u003cspan refid=\"Tab5\" class=\"InternalRef\"\u003e5\u003c/span\u003e). The treatments also influenced the demographic parameters highlighted in the fertility life table (Table\u0026nbsp;\u003cspan refid=\"Tab6\" class=\"InternalRef\"\u003e6\u003c/span\u003e). Anosom\u0026reg; presented the lowest intrinsic rate of growth (\u003cem\u003erₘ\u003c/em\u003e = 0.039), significantly lower than the control (0.05), Azamax\u0026reg; (0.058), and Premio\u0026reg; (0.052). The net reproductive rate (\u003cem\u003eR\u003c/em\u003e\u003csub\u003e\u003cem\u003e0\u003c/em\u003e\u003c/sub\u003e) increased in the following order: Anosom\u0026reg; (8.68), EFAMON (9.82), ESAM (10.64), control (15.77), Premio\u0026reg; (17.61), and Azamax\u0026reg; (21.66). A similar pattern was observed for the finite rate of increase (\u003cem\u003eλ\u003c/em\u003e). No statistical differences were observed for the mean generation time (\u003cem\u003eT\u003c/em\u003e).\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab4\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 4\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eMean (\u0026plusmn;\u0026thinsp;SE) development time and sex ratio of the F\u003csub\u003e1\u003c/sub\u003e generation of \u003cem\u003eD. luteipes\u003c/em\u003e exposed to synthetic and botanical insecticides\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"8\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c5\" colnum=\"5\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c6\" colnum=\"6\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c7\" colnum=\"7\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c8\" colnum=\"8\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003eTreatments\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colspan=\"6\" nameend=\"c7\" namest=\"c2\"\u003e \u003cp\u003eTime development (days)\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c8\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003eSexual\u003c/p\u003e \u003cp\u003eRatio\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003eEgg\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c3\"\u003e \u003cp\u003e1st\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c4\"\u003e \u003cp\u003e2nd\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c5\"\u003e \u003cp\u003e3rd\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c6\"\u003e \u003cp\u003e4th\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c7\"\u003e \u003cp\u003eEgg-adult\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eControl\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e8.65\u0026thinsp;\u0026plusmn;\u0026thinsp;0.18\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e8.00\u0026thinsp;\u0026plusmn;\u0026thinsp;0.26\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e5.50\u0026thinsp;\u0026plusmn;\u0026thinsp;0.26\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e6.37\u0026thinsp;\u0026plusmn;\u0026thinsp;0.37\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e8.00\u0026thinsp;\u0026plusmn;\u0026thinsp;0.32\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e36.50\u0026thinsp;\u0026plusmn;\u0026thinsp;0.53\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e0.51\u0026thinsp;\u0026plusmn;\u0026thinsp;0.05\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eEFAMON\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e8.62\u0026thinsp;\u0026plusmn;\u0026thinsp;0.18\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e8.25\u0026thinsp;\u0026plusmn;\u0026thinsp;0.16\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e6.14\u0026thinsp;\u0026plusmn;\u0026thinsp;0.26\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e6.57\u0026thinsp;\u0026plusmn;\u0026thinsp;0.52\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e7.20\u0026thinsp;\u0026plusmn;\u0026thinsp;0.37\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e37.66\u0026thinsp;\u0026plusmn;\u0026thinsp;0.84\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e0.61\u0026thinsp;\u0026plusmn;\u0026thinsp;0.06\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eESAM\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e8.5\u0026thinsp;\u0026plusmn;\u0026thinsp;0.22\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e8.5\u0026thinsp;\u0026plusmn;\u0026thinsp;0.22\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e6.0\u0026thinsp;\u0026plusmn;\u0026thinsp;0.36\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e6.6\u0026thinsp;\u0026plusmn;\u0026thinsp;0.49\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e7.83\u0026thinsp;\u0026plusmn;\u0026thinsp;0.30\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e37.5\u0026thinsp;\u0026plusmn;\u0026thinsp;0.5\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e0.51\u0026thinsp;\u0026plusmn;\u0026thinsp;0.07\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eAnosom\u0026reg;\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e8.85\u0026thinsp;\u0026plusmn;\u0026thinsp;0.14\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e8.57\u0026thinsp;\u0026plusmn;\u0026thinsp;0.29\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e6.00\u0026thinsp;\u0026plusmn;\u0026thinsp;0.21\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e5.85\u0026thinsp;\u0026plusmn;\u0026thinsp;0.26\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e8.00\u0026thinsp;\u0026plusmn;\u0026thinsp;0.30\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e37.28\u0026thinsp;\u0026plusmn;\u0026thinsp;0.47\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e0.47\u0026thinsp;\u0026plusmn;\u0026thinsp;0.04\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eAzamax\u0026reg;\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e8.50\u0026thinsp;\u0026plusmn;\u0026thinsp;0.18\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e8.62\u0026thinsp;\u0026plusmn;\u0026thinsp;0.18\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e5.25\u0026thinsp;\u0026plusmn;\u0026thinsp;0.31\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e6.25\u0026thinsp;\u0026plusmn;\u0026thinsp;0.31\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e8.00\u0026thinsp;\u0026plusmn;\u0026thinsp;0.37\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e36.65\u0026thinsp;\u0026plusmn;\u0026thinsp;0.26\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e0.52\u0026thinsp;\u0026plusmn;\u0026thinsp;0.06\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003ePremio\u0026reg;\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e8.42\u0026thinsp;\u0026plusmn;\u0026thinsp;0.20\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e8.28\u0026thinsp;\u0026plusmn;\u0026thinsp;0.18\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e5.71\u0026thinsp;\u0026plusmn;\u0026thinsp;0.18\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e6.33\u0026thinsp;\u0026plusmn;\u0026thinsp;0.33\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e7.16\u0026thinsp;\u0026plusmn;\u0026thinsp;0.47\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e36.00\u0026thinsp;\u0026plusmn;\u0026thinsp;0.25\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e0.51\u0026thinsp;\u0026plusmn;\u0026thinsp;0.21\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eF\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e0.62\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e1.17\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e1.63\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e0.52\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e1.13\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e1.58\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e0.46\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003ep\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e0.68\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e0.34\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e0.17\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e0.76\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e0.36\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e0.19\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e0.80\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cp\u003eEFAMON (aqueous emulsion of the methanolic fraction of the ethanolic extract of \u003cem\u003eAnnona montana\u003c/em\u003e leaves); ESAM (aqueous emulsion of the ethanolic extract of \u003cem\u003eAnnona mucosa\u003c/em\u003e seeds); Anosom\u0026reg; (acetogenin annonin); Azamax\u0026reg; (azadirachtin\u0026thinsp;+\u0026thinsp;3-tigloylazadirachtol); Premio\u0026reg; (chlorantraniliprole)\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab5\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 5\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eViability (%) of eggs and immature stages of the F\u003csub\u003e1\u003c/sub\u003e generation of \u003cem\u003eD. luteipes\u003c/em\u003e exposed to synthetic and botanical insecticides\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"7\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c5\" colnum=\"5\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c6\" colnum=\"6\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c7\" colnum=\"7\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003eTreatments\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colspan=\"6\" nameend=\"c7\" namest=\"c2\"\u003e \u003cp\u003eViability (%)\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003eEgg\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c3\"\u003e \u003cp\u003e1st\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c4\"\u003e \u003cp\u003e2nd\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c5\"\u003e \u003cp\u003e3rd\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c6\"\u003e \u003cp\u003e4th\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c7\"\u003e \u003cp\u003eTotal\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eControl\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e73.41\u0026thinsp;\u0026plusmn;\u0026thinsp;7.23\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e87.01\u0026thinsp;\u0026plusmn;\u0026thinsp;4.56\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e91.83\u0026thinsp;\u0026plusmn;\u0026thinsp;3.12\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e95.52\u0026thinsp;\u0026plusmn;\u0026thinsp;2.13\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e91.91\u0026thinsp;\u0026plusmn;\u0026thinsp;4.76a\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c7\"\u003e \u003cp\u003e52.747.76\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eEFAMON\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e69.46\u0026thinsp;\u0026plusmn;\u0026thinsp;6.60\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e89.68\u0026thinsp;\u0026plusmn;\u0026thinsp;3.97\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e91.62\u0026thinsp;\u0026plusmn;\u0026thinsp;3.60\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e76.46\u0026thinsp;\u0026plusmn;\u0026thinsp;12.85\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e54.54\u0026thinsp;\u0026plusmn;\u0026thinsp;11.50b\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c7\"\u003e \u003cp\u003e27.27\u0026thinsp;\u0026plusmn;\u0026thinsp;8.25\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eESAM\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e87.34\u0026thinsp;\u0026plusmn;\u0026thinsp;5.50\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e86.31\u0026thinsp;\u0026plusmn;\u0026thinsp;10.41\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e88.05\u0026thinsp;\u0026plusmn;\u0026thinsp;4.12\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e84.07\u0026thinsp;\u0026plusmn;\u0026thinsp;3.07\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e74.36\u0026thinsp;\u0026plusmn;\u0026thinsp;5.96ab\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c7\"\u003e \u003cp\u003e39.5\u0026thinsp;\u0026plusmn;\u0026thinsp;4.82\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eAnosom\u0026reg;\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e55.76\u0026thinsp;\u0026plusmn;\u0026thinsp;11.76\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e91.29\u0026thinsp;\u0026plusmn;\u0026thinsp;3.23\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e96.08\u0026thinsp;\u0026plusmn;\u0026thinsp;1.74\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e97.17\u0026thinsp;\u0026plusmn;\u0026thinsp;2.06\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e93.56\u0026thinsp;\u0026plusmn;\u0026thinsp;4.78a\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c7\"\u003e \u003cp\u003e46.51\u0026thinsp;\u0026plusmn;\u0026thinsp;11.35\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eAzamax\u0026reg;\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e77.29\u0026thinsp;\u0026plusmn;\u0026thinsp;7.73\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e85.58\u0026thinsp;\u0026plusmn;\u0026thinsp;4.46\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e96.91\u0026thinsp;\u0026plusmn;\u0026thinsp;1.72\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e89.18\u0026thinsp;\u0026plusmn;\u0026thinsp;4.67\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e74.31\u0026thinsp;\u0026plusmn;\u0026thinsp;5.33ab\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c7\"\u003e \u003cp\u003e41.34\u0026thinsp;\u0026plusmn;\u0026thinsp;5.18\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003ePremio\u0026reg;\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e88.49\u0026thinsp;\u0026plusmn;\u0026thinsp;6.58\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e90.92\u0026thinsp;\u0026plusmn;\u0026thinsp;4.12\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e84.38\u0026thinsp;\u0026plusmn;\u0026thinsp;5.40\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e85.71\u0026thinsp;\u0026plusmn;\u0026thinsp;14.29\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e86.87\u0026thinsp;\u0026plusmn;\u0026thinsp;6.32a\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c7\"\u003e \u003cp\u003e53.84\u0026thinsp;\u0026plusmn;\u0026thinsp;12.81\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eF\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e2.24\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e0.22\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e1.92\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e0.89\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e4.74\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c7\"\u003e \u003cp\u003e1.30\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003ep\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e0.07\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e0.95\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e0.11\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e0.49\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e\u0026lt;\u0026thinsp;0.01\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c7\"\u003e \u003cp\u003e0.28\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cp\u003eMeans (\u0026plusmn;\u0026thinsp;SE) followed by the same letter in the column do not differ statistically from each other (Tukey \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.05). EFAMON (aqueous emulsion of the methanolic fraction of the ethanolic extract of \u003cem\u003eAnnona montana\u003c/em\u003e leaves); ESAM (aqueous emulsion of the ethanolic extract of \u003cem\u003eAnnona mucosa\u003c/em\u003e seeds); Anosom\u0026reg; (acetogenin annonin); Azamax\u0026reg; (azadirachtin\u0026thinsp;+\u0026thinsp;3-tigloylazadirachtol); Premio\u0026reg; (chlorantraniliprole)\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab6\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 6\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003ePopulation parameters of \u003cem\u003eD. luteipes\u003c/em\u003e (F\u003csub\u003e1\u003c/sub\u003e) originated from adults exposed to botanical and synthetic insecticides\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"5\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c5\" colnum=\"5\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003eTreatments\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colspan=\"4\" nameend=\"c5\" namest=\"c2\"\u003e \u003cp\u003eDemographic parameter\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003e\u003cem\u003er\u003c/em\u003e\u003csub\u003e\u003cem\u003em\u003c/em\u003e\u003c/sub\u003e\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c3\"\u003e \u003cp\u003e\u003cem\u003eR\u003c/em\u003e\u003csub\u003e\u003cem\u003e0\u003c/em\u003e\u003c/sub\u003e\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c4\"\u003e \u003cp\u003e\u003cem\u003eT\u003c/em\u003e\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c5\"\u003e \u003cp\u003e\u003cem\u003eλ\u003c/em\u003e\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eControl\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e0.050\u0026thinsp;\u0026plusmn;\u0026thinsp;0.001ab\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e15.77\u0026thinsp;\u0026plusmn;\u0026thinsp;1.70abc\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e55.183\u0026thinsp;\u0026plusmn;\u0026thinsp;1.041a\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e1.051\u0026thinsp;\u0026plusmn;\u0026thinsp;0.001ab\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eEFAMON\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e0.042\u0026thinsp;\u0026plusmn;\u0026thinsp;0.002bc\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e9.82\u0026thinsp;\u0026plusmn;\u0026thinsp;1.33c\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e54.603\u0026thinsp;\u0026plusmn;\u0026thinsp;1.397a\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e1.043\u0026thinsp;\u0026plusmn;\u0026thinsp;0.002bc\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eESAM\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e0.041\u0026thinsp;\u0026plusmn;\u0026thinsp;0.002bc\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e10.64\u0026thinsp;\u0026plusmn;\u0026thinsp;2.11bc\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e58.310\u0026thinsp;\u0026plusmn;\u0026thinsp;2.29a\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e1.042\u0026thinsp;\u0026plusmn;\u0026thinsp;0.002bc\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eAnosom\u0026reg;\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e0.039\u0026thinsp;\u0026plusmn;\u0026thinsp;0.003c\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e8.68\u0026thinsp;\u0026plusmn;\u0026thinsp;1.74c\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e55.809\u0026thinsp;\u0026plusmn;\u0026thinsp;2.141a\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e1.040\u0026thinsp;\u0026plusmn;\u0026thinsp;0.004c\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eAzamax\u0026reg;\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e0.058\u0026thinsp;\u0026plusmn;\u0026thinsp;0.001a\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e21.66\u0026thinsp;\u0026plusmn;\u0026thinsp;1.70a\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e53.025\u0026thinsp;\u0026plusmn;\u0026thinsp;0.87a\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e1.060\u0026thinsp;\u0026plusmn;\u0026thinsp;0.001a\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003ePremio\u0026reg;\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e0.052\u0026thinsp;\u0026plusmn;\u0026thinsp;0.002a\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e17.61\u0026thinsp;\u0026plusmn;\u0026thinsp;1.98ab\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e55.051\u0026thinsp;\u0026plusmn;\u0026thinsp;1.263a\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e1.054\u0026thinsp;\u0026plusmn;\u0026thinsp;0.002a\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eF\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e11.85\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e8.66\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e1.03\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e11.99\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003ep\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e\u0026lt;\u0026thinsp;0.001\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e\u0026lt;\u0026thinsp;0.001\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e0.41\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e\u0026lt;\u0026thinsp;0.001\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003ctfoot\u003e \u003ctr\u003e\u003ctd colspan=\"5\"\u003eMeans (\u0026plusmn;\u0026thinsp;SE) followed by the same letter in the column do not differ statistically from each other (Tukey \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.05). (\u003cem\u003er\u003c/em\u003e\u003csub\u003e\u003cem\u003em\u003c/em\u003e\u003c/sub\u003e = intrinsic rate of increase, \u003cem\u003eR\u003c/em\u003e\u003csub\u003e\u003cem\u003e0\u003c/em\u003e\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;net reproductive rate, \u003cem\u003eT\u003c/em\u003e\u0026thinsp;=\u0026thinsp;mean generation time and \u003cem\u003eλ\u003c/em\u003e\u0026thinsp;=\u0026thinsp;finite rate of population increase). EFAMON (aqueous emulsion of the methanolic fraction of the ethanolic extract of \u003cem\u003eAnnona montana\u003c/em\u003e leaves); ESAM (aqueous emulsion of the ethanolic extract of \u003cem\u003eAnnona mucosa\u003c/em\u003e seeds); Anosom\u0026reg; (acetogenin annonin); Azamax\u0026reg; (azadirachtin\u0026thinsp;+\u0026thinsp;3-tigloylazadirachtol); Premio\u0026reg; (chlorantraniliprole)\u003c/td\u003e\u003c/tr\u003e \u003c/tfoot\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003c/div\u003e"},{"header":"Discussion","content":"\u003cp\u003eThis study provides significant contributions to the understanding of the selectivity of botanical and organosynthetic insecticides on the predator \u003cem\u003eD. luteipes\u003c/em\u003e. The synthetic insecticide Premio\u0026reg; (chlorantraniliprole) was found to cause high mortality in nymphs, an effect that was not observed in adults. Insecticide tolerance can vary significantly depending on insect\u0026rsquo;s life stage. The immature stages of natural enemies tend to be more susceptible (Stecca et al. 2017; Freitas et al. \u003cspan citationid=\"CR30\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; Musa et al. \u003cspan citationid=\"CR59\" class=\"CitationRef\"\u003e2021\u003c/span\u003e; Potin et al. \u003cspan citationid=\"CR67\" class=\"CitationRef\"\u003e2022\u003c/span\u003e). This observation can be explained by two factors: 1) the higher ability of the insecticide to penetrate the bodies of nymphs, as their exoskeletons are less sclerotized compared to that of adults (Andersen \u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e2010\u003c/span\u003e, \u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e2012\u003c/span\u003e; Pang et al. \u003cspan citationid=\"CR65\" class=\"CitationRef\"\u003e2023\u003c/span\u003e); 2) the high metabolic cost of detoxifying xenobiotics (M\u0026uuml;ller \u003cspan citationid=\"CR58\" class=\"CitationRef\"\u003e2018\u003c/span\u003e; Khan et al. \u003cspan citationid=\"CR44\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). Insects have detoxification mechanisms to eliminate harmful compounds; however, nymphs may compromise vital resources for their physiological survival by allocating energy to detoxification (Ferreira et al. \u003cspan citationid=\"CR28\" class=\"CitationRef\"\u003e2013\u003c/span\u003e; Luong and Horn \u003cspan citationid=\"CR48\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; Khan et al. \u003cspan citationid=\"CR44\" class=\"CitationRef\"\u003e2021\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eIn a similar study conducted by Freitas et al. (\u003cspan citationid=\"CR30\" class=\"CitationRef\"\u003e2017\u003c/span\u003e), it was observed that nymphs (1st, 2nd, and 4th instars) of \u003cem\u003eD. luteipes\u003c/em\u003e exposed to chlorantraniliprole residues at the label-recommended concentration had their survival affected, which is consistent with the results of our study. Another study by Campos et al. (\u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e2011\u003c/span\u003e) demonstrated that chlorantraniliprole does not cause adult mortality. In another species of Dermaptera, \u003cem\u003eEuborelia annulipes\u003c/em\u003e, chlorantraniliprole showed no toxicity in either adult or third-instar nymphs (Potin et al. \u003cspan citationid=\"CR67\" class=\"CitationRef\"\u003e2022\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eThe botanical insecticides ESAM (aqueous emulsion of the ethanolic extract of \u003cem\u003eAnnona mucosa\u003c/em\u003e seeds) and Anosom\u0026reg; (acetogenin annonin) caused high mortality in first-instar nymphs. These two botanical insecticides are derived from plants of the Annonaceae family, known for biosynthesizing acetogenins (ACGs), which have documented insecticidal activities against various pest insect species (Ansante et al. \u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e2015\u003c/span\u003e, \u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; Ribeiro, et al. \u003cspan citationid=\"CR70\" class=\"CitationRef\"\u003e2015\u003c/span\u003e; Souza et al. \u003cspan citationid=\"CR80\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; Gomes \u003cspan citationid=\"CR33\" class=\"CitationRef\"\u003e2018\u003c/span\u003e; Hidalgoa et al. \u003cspan citationid=\"CR40\" class=\"CitationRef\"\u003e2020\u003c/span\u003e). Their modes of action include inhibiting complex I of the mitochondrial electron transport system, preventing ATP production, and induction of programmed cell death (Alali et al. \u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e1999\u003c/span\u003e; Tormo et al. \u003cspan citationid=\"CR85\" class=\"CitationRef\"\u003e1999\u003c/span\u003e). Recent studies have also demonstrated the effects of acetogenins on the digestive system of certain insects, reducing nutrient absorption (Costa et al. \u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e2016\u003c/span\u003e; Machado et al. \u003cspan citationid=\"CR49\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). Additionally, the interaction of acetogenins with cell membrane phosphates represents a novel site of action, leading to dehydration and causing irreversible damage to their structure and biological functions (Bombasaro et al. \u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e2011\u003c/span\u003e; Blessing et al. 2012). Thus, first-instar nymphs may be more vulnerable to these compounds due to their lower exoskeleton sclerotization and high metabolic demand for detoxification, which may explain the higher observed mortality (Andersen \u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e2010\u003c/span\u003e, \u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e2012\u003c/span\u003e; Ferreira et al. \u003cspan citationid=\"CR28\" class=\"CitationRef\"\u003e2013\u003c/span\u003e; M\u0026uuml;ller \u003cspan citationid=\"CR58\" class=\"CitationRef\"\u003e2018\u003c/span\u003e; Pang et al. \u003cspan citationid=\"CR65\" class=\"CitationRef\"\u003e2023\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eEvaluating the sublethal impact of insecticides on the predation capacity and locomotion behavior of predators ensures that these biological control agents can continue to fulfill their ecological roles (Desneux et al. \u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e2007\u003c/span\u003e). Although the survival of adult \u003cem\u003eD. luteipes\u003c/em\u003e was not affected by the treatments, the synthetic insecticide Premio\u0026reg; (chlorantraniliprole) significantly reduced prey consumption and walking velocity. Predation is the primary ecological function of these insects, and changes in locomotion behavior may compromise their predatory efficacy, negatively affecting pest control capabilities (Campos et al. \u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e2011\u003c/span\u003e; Freitas et al. \u003cspan citationid=\"CR30\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; He et al. \u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e2019\u003c/span\u003e; Moreira et al. \u003cspan citationid=\"CR56\" class=\"CitationRef\"\u003e2023\u003c/span\u003e; Silva et al. \u003cspan citationid=\"CR78\" class=\"CitationRef\"\u003e2023\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eChlorantraniliprole is a ryanodine receptor modulator that affects muscle calcium release (Nauen \u003cspan citationid=\"CR61\" class=\"CitationRef\"\u003e2006\u003c/span\u003e; Lahm et al. \u003cspan citationid=\"CR45\" class=\"CitationRef\"\u003e2009\u003c/span\u003e). This insecticide can impact all muscles, including those related to locomotion, thus affecting insect movement and, consequently, their predation capability (He et al. \u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). Similar outcomes were observed in a study by Freitas et al. (\u003cspan citationid=\"CR30\" class=\"CitationRef\"\u003e2017\u003c/span\u003e), where the locomotion behavior of \u003cem\u003eD. luteipes\u003c/em\u003e was reduced following exposure to chlorantraniliprole. Other studies support our findings regarding predation capacity. In \u003cem\u003eEuborellia annulipes\u003c/em\u003e (Dermaptera: Anisolabididae), predation significantly decreases after chlorantraniliprole exposure (Potin et al. \u003cspan citationid=\"CR67\" class=\"CitationRef\"\u003e2022\u003c/span\u003e). This impairment has also been observed in other natural enemies (Musa et al. \u003cspan citationid=\"CR59\" class=\"CitationRef\"\u003e2021\u003c/span\u003e; Moreira et al. \u003cspan citationid=\"CR56\" class=\"CitationRef\"\u003e2023\u003c/span\u003e). In contrast, Campos et al. (\u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e2011\u003c/span\u003e) showed that this insecticide does not affect the predation capacity of \u003cem\u003eD. luteipes\u003c/em\u003e.\u003c/p\u003e \u003cp\u003eThe botanical insecticide ESAM (aqueous emulsion of the ethanolic extract of \u003cem\u003eAnnona mucosa\u003c/em\u003e seeds) and Premio\u0026reg; (chlorantraniliprole) reduced the average longevity of adults. Regarding reproductive parameters, Premio\u0026reg; accelerated the pre-oviposition period, whereas fecundity was unaffected by any treatment. Literature suggests that reproduction is an energetically costly activity (Tallamy and Denno \u003cspan citationid=\"CR83\" class=\"CitationRef\"\u003e1982\u003c/span\u003e; Soulages \u003cspan citationid=\"CR79\" class=\"CitationRef\"\u003e2010\u003c/span\u003e; De Loof \u003cspan citationid=\"CR24\" class=\"CitationRef\"\u003e2011\u003c/span\u003e). In this study, the number of eggs per female was not influenced; however, insects exposed to ESAM and Premio\u0026reg; had shorter lives. This suggests a possible trade-off: insects exposed to these compounds had their physiological survival activities affected while maintaining reproductive capacity (Blacher et al. \u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; Jiang et al. \u003cspan citationid=\"CR42\" class=\"CitationRef\"\u003e2023\u003c/span\u003e). Additionally, the stress caused by Premio\u0026reg; may accelerate the reproductive cycle in females. Similarly, this stress might respond to the toxic environment, inducing females to oviposit earlier as a survival strategy without necessarily reducing their total egg production (Fogel et al. \u003cspan citationid=\"CR29\" class=\"CitationRef\"\u003e2016\u003c/span\u003e; Sial et al. \u003cspan citationid=\"CR76\" class=\"CitationRef\"\u003e2018\u003c/span\u003e; Azhar and Khan \u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e2024\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eFreitas et al. (\u003cspan citationid=\"CR30\" class=\"CitationRef\"\u003e2017\u003c/span\u003e) demonstrated that only 20% of \u003cem\u003eD. luteipes\u003c/em\u003e adults that came into contact with chlorantraniliprole residues survived up to 50 days. Other predators, such as \u003cem\u003eChrysoperla\u003c/em\u003e spp., also had their longevity affected by this insecticide (Wankhade et al. \u003cspan citationid=\"CR89\" class=\"CitationRef\"\u003e2020\u003c/span\u003e). However, chlorantraniliprole did not affect the fecundity of \u003cem\u003eCoccinella septempunctata\u003c/em\u003e (Coleoptera: Coccinellidae) at the lowest tested dose (Cong et al. \u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e2023\u003c/span\u003e). Similar results were obtained for \u003cem\u003eColeomegilla quadrifasciata\u003c/em\u003e (Coleoptera: Coccinellidae) when exposed to dry chlorantraniliprole residues (Silva et al. \u003cspan citationid=\"CR77\" class=\"CitationRef\"\u003e2020\u003c/span\u003e). In contrast, He et al. (\u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e2019\u003c/span\u003e) observed that applying the recommended field dose of chlorantraniliprole to \u003cem\u003eC. septempunctata\u003c/em\u003e reduced fecundity. These results indicate that for \u003cem\u003eD. luteipes\u003c/em\u003e, the lethal concentration (LC\u003csub\u003e90\u003c/sub\u003e) of chlorantraniliprole-based insecticide used in this study did not cause changes in fecundity. In contrast, the effects may differ for other predator groups.\u003c/p\u003e \u003cp\u003eIn addition to the direct impacts of insecticides, the effects of previous exposure can be transmitted to subsequent generations (Cheng et al. \u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e2022\u003c/span\u003e; Afza et al. \u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2023\u003c/span\u003e). Therefore, selectivity studies must include an evaluation of the transgenerational effects (Le et al. \u003cspan citationid=\"CR46\" class=\"CitationRef\"\u003e2021\u003c/span\u003e; Moreira et al. \u003cspan citationid=\"CR56\" class=\"CitationRef\"\u003e2023\u003c/span\u003e). In this study, parameters such as developmental time, viability of developmental stages, sex ratio, and demographic parameters of the F\u003csub\u003e1\u003c/sub\u003e generation were evaluated.\u003c/p\u003e \u003cp\u003eThe development time of each stage of \u003cem\u003eD. luteipes\u003c/em\u003e and sex ratio were not influenced by the treatments. Similar results were found by Potin et al. (\u003cspan citationid=\"CR67\" class=\"CitationRef\"\u003e2022\u003c/span\u003e), who studied the effect of chlorantraniliprole on \u003cem\u003eEuborellia annulipes\u003c/em\u003e (Dermaptera: Anisolabididae) and observed no impact on development time. Additionally, Abreu et al. (\u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e2024\u003c/span\u003e) investigated the selectivity of different aqueous extracts on the duration and fecundity of \u003cem\u003eMarava arachidis\u003c/em\u003e (Dermaptera: Labiidae) and demonstrated that, at a concentration of 10% (w v\u003csup\u003e\u0026minus;\u0026thinsp;1\u003c/sup\u003e), the extracts did not affect this species.\u003c/p\u003e \u003cp\u003eOnly the viability of the fourth-instar nymphs was influenced by the treatments, with the botanical insecticide EFAMON causing the lowest viability. No study has demonstrated the effects of \u003cem\u003eA. montana\u003c/em\u003e derivatives on natural enemies. However, this plant belongs to the same genus as other \u003cem\u003eAnnona\u003c/em\u003e species, whose extracts have been shown to affect the viability of various insect species (Bernardi et al. \u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; Souza et al. \u003cspan citationid=\"CR81\" class=\"CitationRef\"\u003e2019\u003c/span\u003e; Gon\u0026ccedil;alves et al. \u003cspan citationid=\"CR34\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). Much of this effect is attributed to the compounds in its composition, such as alkaloids, acetogenins, triterpenes, steroids, and lignans. Among these, acetogenins are particularly noteworthy, with their possible modes of action described earlier in this study (Gomes \u003cspan citationid=\"CR33\" class=\"CitationRef\"\u003e2018\u003c/span\u003e; Hidalgoa et al. \u003cspan citationid=\"CR40\" class=\"CitationRef\"\u003e2020\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eOne approach to assess the impact of insecticides on insect population dynamics is to use fertility life tables (Amarasekare et al. \u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e2016\u003c/span\u003e; Rossini et al. \u003cspan citationid=\"CR73\" class=\"CitationRef\"\u003e2024\u003c/span\u003e). This study revealed that the F\u003csub\u003e1\u003c/sub\u003e generation, whose parents were exposed to Anosom\u0026reg; (acetogenin annonin) treatment, showed lower values of intrinsic growth rate (\u003cem\u003er\u003c/em\u003e\u003csub\u003e\u003cem\u003em\u003c/em\u003e\u003c/sub\u003e) and finite rate of increase (\u003cem\u003eλ\u003c/em\u003e) than the control. These parameters consider data on female fecundity and survival, which may indicate potential future effects on population dynamics, although not statistically different in this study (Kakde et al. \u003cspan citationid=\"CR43\" class=\"CitationRef\"\u003e2014\u003c/span\u003e). The intrinsic population growth rate (\u003cem\u003er\u003c/em\u003e\u003csub\u003e\u003cem\u003em\u003c/em\u003e\u003c/sub\u003e) reflects the maximum growth rate of a population, with higher values indicating a more significant potential for population success. The finite rate of increase represents the population growth rate from one generation to the next, and both parameters indicate whether the population is growing, stable, or declining (Maia et al. \u003cspan citationid=\"CR50\" class=\"CitationRef\"\u003e2000\u003c/span\u003e). A similar result was observed by Morais (\u003cspan citationid=\"CR54\" class=\"CitationRef\"\u003e2020\u003c/span\u003e), who demonstrated a reduction in the fecundity of the predator \u003cem\u003eCryptolaemus montrouzieri\u003c/em\u003e (Coleoptera: Coccinellidae) when exposed to the same treatment. This suggests that Anosom\u0026reg; may have significant effects on population dynamics.\u003c/p\u003e \u003cp\u003eThe results of this study indicate that the botanical insecticides, particularly a formulation based on limonoids (Azamax\u0026reg;) and an emulsion of the methanolic fraction of the ethanolic extract of \u003cem\u003eAnnona montana\u003c/em\u003e leaves (EFAMON), are less lethal to the natural enemy \u003cem\u003eD. luteipes\u003c/em\u003e than synthetic insecticide chlorantraniliprole (Premio\u0026reg;). Chlorantraniliprole exhibited high toxicity, negatively impacting the mortality, predation capacity, and walking behavior of \u003cem\u003eD. luteipes\u003c/em\u003e. These findings suggest that the botanical insecticides tested may be more compatible with conserving the studied natural enemy. However, there is no simple answer when it comes to selectivity studies. While botanical insecticides have demonstrated reduced effects on certain parameters, the results have varied for others. This lack of a definitive response is expected, as selectivity studies are complementary and build upon each other. Future investigations, particularly ecotoxicological assessments conducted under field conditions, can provide a more comprehensive understanding based on the results obtained. Therefore, the findings of this research offer significant contributions to filling the gaps in compatibility between chemical and biological control, promoting more sustainable agricultural practices.\u003c/p\u003e"},{"header":"Declarations","content":"\u003cp\u003e\u003cstrong\u003eAuthor contributions\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eEDRS: conceptualization, methodology, statistical analysis, writing original draft; LVT: methodology, statistical analysis; MY, GSR, and IB: methodology and review; PTY: conceptualization, writing review and editing; LPR: writing review and editing. All authors reviewed and approved the manuscript\u003cstrong\u003e.\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eFunding\u0026nbsp;\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThis research was funded by Coordena\u0026ccedil;\u0026atilde;o de Aperfei\u0026ccedil;oamento de Pessoal de N\u0026iacute;vel Superior \u0026ndash; Brasil (CAPES) \u0026ndash; Finance code 001.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eConflict of interest\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe authors declare no competing interests\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eEthics approval\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eNot applicable\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\n\u003cli\u003eAbreu KG, Brito CH de, Filho MC de O et al (2024) Physiological selectivity of aqueous extracts on nymphs and adults of \u003cem\u003eMarava arachidis\u003c/em\u003e (Dermaptera: Labiidae). Rev Principia - Divulg Cient\u0026iacute;fica e Tecnol\u0026oacute;gica do IFPB. https://doi.org/doi:http://dx.doi.org/10.18265/1517-0306a2022id7259.\u003c/li\u003e\n\u003cli\u003eAfza R, Afzal A, Riaz MA et al (2023) Sublethal and transgenerational effects of synthetic insecticides on the biological parameters and functional response of \u003cem\u003eCoccinella septempunctata\u003c/em\u003e (Coleoptera : Coccinellidae) under laboratory conditions. Front Physiol 14:1\u0026ndash;14. https://doi.org/10.3389/fphys.2023.1088712\u003c/li\u003e\n\u003cli\u003eAlali FQ, Liu X, Mclaughlin JL (1999) Annonaceous Acetogenins : Recent Progress. J Nat Prod 62:504\u0026ndash;540\u003c/li\u003e\n\u003cli\u003eAmarasekare KG, Shearer PW, Mills NJ (2016) Testing the selectivity of pesticide effects on natural enemies in laboratory bioassays. 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Thesis, Universidade Federal de Alagoas\u003c/li\u003e\n\u003cli\u003eGon\u0026ccedil;alves GLP, Ribeiro L do P, Vendramim JD (2021) Toxicities of \u003cem\u003eAnnona\u003c/em\u003e derivatives and semi-purified fractions against \u003cem\u003eZabrotes subfasciatus\u003c/em\u003e. Trop Subtrop Agroecosystems 24:115\u0026ndash;124\u003c/li\u003e\n\u003cli\u003eGontijo LM, Celestino D, Queiroz OS et al (2015) Impacts of azadirachtin and chlorantraniliprole on the developmental stages of pirate bug predators (Hemiptera: Anthocoridae) of the tomato pinworm \u003cem\u003eTuta absoluta\u003c/em\u003e (Lepidoptera: Gelechiidae). Florida Entomol 98:59\u0026ndash;64. https://doi.org/10.1653/024.098.0111\u003c/li\u003e\n\u003cli\u003eGreene GL, Leppla NC, Dickerson WA (1976) Velvetbean Caterpillar: A Rearing Procedure and Artificial Medium123. J Econ Entomol 69:487\u0026ndash;488. https://doi.org/10.1093/jee/69.4.487\u003c/li\u003e\n\u003cli\u003eGuimar\u0026atilde;es MRF, Silva RB, Figueiredo MDLC (2006) Avan\u0026ccedil;os na Metodologia de Cria\u0026ccedil;\u0026atilde;o de \u003cem\u003eDoru luteipes\u003c/em\u003e (Scudder, 1876) (Dermaptera: Forficulidae). In: Congresso Nacional de Milho e Sorgo. Belo Horizonte, Minas Gerais, p 7\u003c/li\u003e\n\u003cli\u003eHaddi K, Turchen LM, Jumbo OV et al (2020) Rethinking biorational insecticides for pest management : unintended effects and consequences. Pest Manag Sci 76:2286\u0026ndash;2293. https://doi.org/10.1002/ps.5837\u003c/li\u003e\n\u003cli\u003eHe F, Sun S, Tan H et al (2019) Compatibility of chlorantraniliprole with the generalist predator \u003cem\u003eCoccinella septempunctata\u003c/em\u003e L. (Coleoptera:Coccinellidae) based toxicity, life-cycle development and population parameters in laboratory microcosms. 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Springer, Cham, pp 63\u0026ndash;69\u003c/li\u003e\n\u003cli\u003eWankhade S V, Sawai HR, Chaure PR, Renuka D (2020) Comparative effects of insecticides on mortality , longevity and fecundity of \u003cem\u003eChrysoperla\u003c/em\u003e spp . ( Neuroptera : Chrysopidae ). J Entomol Zool Stud 8:1878\u0026ndash;1882\u003c/li\u003e\n\u003c/ol\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":false,"highlight":"","institution":"","isAcceptedByJournal":true,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":true,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"neotropical-entomology","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"nent","sideBox":"Learn more about [Neotropical Entomology](https://www.springer.com/journal/13744)","snPcode":"13744","submissionUrl":"https://www.editorialmanager.com/nent/default2.aspx","title":"Neotropical Entomology","twitterHandle":"","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"em","reportingPortfolio":"Springer Hybrid","inReviewEnabled":true,"inReviewRevisionsEnabled":false},"keywords":"Non-target organisms, Acetogenins, Limonoids, Biological control, Sublethal effects","lastPublishedDoi":"10.21203/rs.3.rs-5823057/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-5823057/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003eTo achieve sustainability in agricultural pest management, it is essential to integrate chemical and biological control through selectivity studies. In this study, we evaluated the lethal and sublethal effects of both botanical and synthetic insecticides used for controlling the fall armyworm, \u003cem\u003eSpodoptera frugiperda\u003c/em\u003e (J.E. Smith) (Lepidoptera: Noctuidae), on its natural enemy \u003cem\u003eDoru luteipes\u003c/em\u003e (Scudder) (Dermaptera: Forficulidae). For this purpose, bioassays of mortality, behavior, and transgenerational effects were conducted. Botanical insecticides rich in acetogenins and limonoids caused less than 30% mortality in \u003cem\u003eD. luteipes\u003c/em\u003e nymphs (2nd, 3rd, and 4th instars). In contrast, chlorantraniliprole-based insecticide (Premio\u0026reg;) was highly toxic, presenting mortality above 80% at all nymphal stages and reducing predation capacity by 55.97% and walking velocity by 28.44% compared to the control. Aqueous emulsion of the ethanolic extract from \u003cem\u003eAnnona mucosa\u003c/em\u003e seeds (ESAM) reduced the longevity of the adults to 88.88 days. Chlorantraniliprole resulted in the shortest pre-oviposition period (9.44 days), followed by a limonoids-based botanical insecticide (Azamax\u0026reg;) (11.00 days). Fourth-instar nymphs of the F\u003csub\u003e1\u003c/sub\u003e generation showed lower viability (54.54%) in the treatment with aqueous emulsion of the methanolic fraction from \u003cem\u003eAnnona montana\u003c/em\u003e leaves (EFAMON). The annonin-based commercial botanical insecticide (Anosom\u0026reg;) affected life table parameters, reducing the intrinsic growth rate (\u003cem\u003er\u003c/em\u003e\u003csub\u003e\u003cem\u003em\u003c/em\u003e\u003c/sub\u003e = 0.039) and finite rate of increase (\u003cem\u003eλ\u003c/em\u003e\u0026thinsp;=\u0026thinsp;1.04). These findings indicate that botanical insecticides are less hazardous to the natural enemy \u003cem\u003eD. luteipes\u003c/em\u003e than synthetic insecticide. This study provides important insights for improving pest control while preserving natural enemies.\u003c/p\u003e","manuscriptTitle":"Investigating the selectivity of botanical and synthetic insecticides on Doru luteipes: there is no simple answer","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2025-01-23 10:52:13","doi":"10.21203/rs.3.rs-5823057/v1","editorialEvents":[{"type":"communityComments","content":0},{"type":"reviewerAgreed","content":"","date":"2025-01-23T11:40:59+00:00","index":0,"fulltext":""},{"type":"reviewersInvited","content":"","date":"2025-01-21T15:34:14+00:00","index":"","fulltext":""},{"type":"editorAssigned","content":"","date":"2025-01-14T16:55:52+00:00","index":"","fulltext":""},{"type":"submitted","content":"Neotropical Entomology","date":"2025-01-13T19:56:35+00:00","index":"","fulltext":""}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"neotropical-entomology","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"nent","sideBox":"Learn more about [Neotropical Entomology](https://www.springer.com/journal/13744)","snPcode":"13744","submissionUrl":"https://www.editorialmanager.com/nent/default2.aspx","title":"Neotropical Entomology","twitterHandle":"","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"em","reportingPortfolio":"Springer Hybrid","inReviewEnabled":true,"inReviewRevisionsEnabled":false}}],"origin":"","ownerIdentity":"904ffda2-aeb5-4e9c-85a3-ba6bdeb257c8","owner":[],"postedDate":"January 23rd, 2025","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"under-review","subjectAreas":[],"tags":[],"updatedAt":"2025-05-20T15:02:17+00:00","versionOfRecord":[],"versionCreatedAt":"2025-01-23 10:52:13","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-5823057","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-5823057","identity":"rs-5823057","version":["v1"]},"buildId":"8U1c8b4HqxoKbykW_rLl7","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}