Introduction

Integrated pest management (IPM) uses different control tactics in a concerted manner. The goal is to complement natural, biological forms of pest control and to maintain pest populations below the levels that cause damage, thus conserving the environment and beneficial arthropods. In this goal, parasitoids and agrochemicals can be used simultaneously, provided there is compatibility between these control methods (REISS et al., 1998; POLANCZYK et al., 2010). Thus, the selectivity of insecticides to natural enemies is of great importance and should be evaluated when choosing insecticides for IPM programs (BUENO et al., 2012).

Insecticide selectivity to natural enemies has been studied for decades (HASSAN et al., 1998; ZOTTI et al., 2008; FONSECA et al., 2012; DIAMANTINO et al., 2014). However, in addition to being specific to the biological organism under study and its phases of development, pesticide selectivity is directly related to its concentration (DESNEUX et al., 2004). Changes in dosage can directly impact its selectivity classification (BUENO et al., 2017). Those changes can occur, for example, after occurence of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) in crops in Brazil (CZEPAK et al., 2013), when pesticides started to be used in higher concentrations than those normally recommended for other pest species, since target-pest populations already showed resistance to several insecticides (WYCKHUYS et al., 2013). Thus, such intensified use of insecticides can significantly impact beneficial entomofauna and lead to changes in IPM strategies (BUENO et al., 2008).

Helicoverpa armigera gained attention in soybeans, where it is detrimental throughout the vegetative and reproductive stages of plant development because it consumes leaves and pods (WANG; LI, 1984; CZEPAK et al., 2013). It occurs simultaneously with other important pests, such as the brown stink bug Euschistus heros (Fabricius) (Hemiptera: Pentatomidae). Considering the cultivation of soybeans as a system in which various organisms coexist, the chemical control of H. armigera can impact the natural biological control of other pests. Pesticides can have deleterious effects on the natural enemies of the brown stink bug when nonselective products or abusive pesticide dosages are used (POMARI-FERNANDES et al., 2015).

Among the natural enemies of E. heros, the egg parasitoid Telenomus podisi (Ashmead) (Hymenoptera: Platygastridae) stands out as a species that shows a preference for this stink bug's eggs (CORRÊA-FERREIRA; AZEVEDO, 2002, DOETZER; FOERSTER, 2007). This further reinforces the importance of integrating different control tactics into IPM and the study of the selectivity of new products and/or new dosages.

Among the products used in the management of H. armigera are chlorantraniliprole and a mixture of chlorantraniliprole with lambda-cyhalothrin. However, few studies have assessed the effect of chlorantraniliprole or lambda-cyhalothrin on T. podisi at higher doses that might be used to control H. armigera. Therefore, we evaluated the possible impacts of spraying chlorantraniliprole and lambda-cyhalothrin during the pupal and adult stages of T. podisi and determined the toxicity of different doses of those chemicals.

Materials and Methods

The insects used in the bioassays were taken from laboratory rearing that is maintained in the Embrapa Soybean. The eggs of E. heros that were used in the bioassays were previously stored in liquid nitrogen.

We used an application rate of 150 L ha^-1. The solutions for each treatment (Table 1) were sprayed through a Potter Tower previously calibrated to deposit 1.25 ± 0.25 mg per cm², accordingly standardized protocols recommended by the International Organization for Biological Control (IOBC) (HASSAN et al., 1985).

Selectivity of chlorantraniliprole and chlorantraniliprole + lambda-cyhalothrin to pupae of T. podisi

Cards containing T. podisi pupae inside E. heros eggs (13 days post-parasitism) were sprayed (parasitoids pupae approximately 24 hours before adult emergence). Subsequently, the cards remained in environmental conditions (27 ± 2 °C and 50 ± 10% RH) for 2 hours in order for the insecticide to dry. Thereafter, the cards were transferred to standard IOBC cages (DEGRANDE et al., 2002).

Contact cages proposed by Degrande et al. (2002), with glass panels composing the bottom and the top of the cage, were used. The outer surface of the glass plates was covered with black cardboard paper that had a center square (7 cm × 7 cm) removed. The cards containing T. podisi pupae were inserted into the cages. Twenty-four, 72, and 120 h after the emergence of the parasitoids, new cards were inserted with approximately 70 E. heros eggs. The following parameter were evaluated: emergence of adults (%), parasitism (%) of F₀ generation, and emergence (%) of F₁ generation.

Parasitism capacity of T. podisi adults from pupae sprayed with chlorantraniliprole and chlorantraniliprole + lambda-cyhalothrin

We used four females, which emerged from sprayed eggs (Table 1), per replication for the bioassays. Approximately 40 E. heros eggs were attached to 2.5 cm × 5 cm white paperboard cards. The cards were placed into Duran-type tubes containing droplets of pure honey for parasitoid feeding. They were then given to T. podisi females for parasitism. The tubes were sealed with plastic film and kept in temperature-controlled chambers regulated at 25 ± 2 ºC and 70 ± 10% RH, with a photoperiod of 14/10 hours light/dark. Every 24 hours, the cards were removed and changed. This procedure was repeated daily for a period of 15 days. The cards removed from the tubes were placed into plastic bags and kept in the same environmental conditions as where they were parasitized. We assessed the total number of parasitized eggs per female, lifetime parasitism (%), adult emergence (%), the longevity of parental females (days), and the sex ratio of the parasitoids.

Selectivity of chlorantraniliprole and chlorantraniliprole + lambda-cyhalothrin to T. podisi adults

Glass plates (13 × 13 cm, 2 mm thick) were sprayed with various doses of the products (Table 1). Afterwards, they remained in environmental conditions (27 ± 2 ºC and 50 ± 10% RH) for 2 hours, for complete evaporation of the pesticides, leaving a film of the product on the glass to allow for contact between the parasitoids and the insecticides. In the preparation of cages, the glass plates were covered externally with black cardboard paper, whose central square (7 cm × 7 cm) was removed (DEGRANDE et al., 2002).

Telenomus podisi adults at 48 hours of age were inserted into the contact cage through emergence tubes (CARMO et al., 2009), connected through holes in the cages. The parasitoids were given cards containing 100 non-sprayed E. heros eggs after 24, 72, and 120 hours, to assess the parasitism of the F₀ generation, emergence of adults, and sex ratio of the F₁ generation. Cardstock cards containing honey droplets were placed inside each cage to feed the parasitoids.

Statistical analyses

The experiments were carried out using a completely randomized experimental design, with 10 treatments and five repetitions for each bioassay. The results were submitted to exploratory analyses to evaluate the normality assumptions of the residuals (SHAPIRO and WILK, 1965), the homogeneity of variance of the treatments, and the additivity of the model (BURR and FOSTER, 1972), to apply analysis of variance (ANOVA). The means were compared by the F test or the Tukey test (p ≤ 0.05) (SAS Institute, 2009). In addition, the effect of the treatments on T. podisi was determined by comparison with the negative control (water), calculated with the formula used by Hassan et al. (1985):

Thus, the treatments were classified according to their toxicity: class 1 = innocuous (E < 30%), class 2 = slightly harmful (30% ≤ E < 80), class 3 = moderately harmful (80% ≤ E< 99), and class 4 = noxious (E ≥ 99%) (HASSAN et al., 1985).

Results

Selectivity of chlorantraniliprole and chlorantraniliprole + lambda-cyhalothrin to T. podisi pupae

The largest percentage of T. podisi emergence (79.84%) occurred in the control treatment with water, followed by the lower concentrations of 10 and 15 g active ingredient (a.i.) ha^-1 of chlorantraniliprole, with percentages of 71.34% and 73.53%, respectively. This was followed by the lowest concentration of 10 + 5 g a.i. ha^-1 (chlorantraniliprole + lambda-cyhalothrin), with a percentage of 70.86% (Table 2). The emergence percentages were 66.00%, 67.02%, and 63.28% at the highest concentrations of 20, 30, and 50 g a.i. ha^-1 of chlorantraniliprole, respectively. The mixture of 20 + 10 g a.i. ha^-1 (chlorantraniliprole + lambda-cyhalothrin) had a percentage of 64.73%. The mixture with higher concentrations of chlorantraniliprole + lambda-cyhalothrin (30 + 15 g a.i. ha^-1) resulted in 54.05% emergence. The lowest percentage of emergence was observed in the chlorpyrifos treatment (51.09%) (Table 2).

For the percentage of parasitism of adults that emerged from sprayed pupae, for all periods tested, the chlorpyrifos spray resulted in the lowest values. These values were 28.24%, 29.12%, and 16.85%, respectively, at 24, 72, and 120 hours. The percentage of parasitism 24 hours after emergence was higher for the water treatment (77.48%) and for 20 g a.i. ha^-1 of chlorantraniliprole (73.48%). Chlorantraniliprole at 50 g a.i. ha^-1 resulted in a lower percentage of parasitism at 53.12% (Table 3).

At 72 hours after emergence, the highest percentage of parasitism was observed in the treatment with 15 g a.i. ha^-1 of chlorantraniliprole (77.4%). For chlorantraniliprole at 50 g a.i. ha^-1, a lower percentage of parasitism was observed: 52.93%. The other treatments ranged from 58.28% for the mixture of chlorantraniliprole + lambda-cyhalothrin at 30 + 15 g a.i. ha^-1, to 69.4% for 10 + 5 g a.i. ha^-1. For parasitism at 120 hours, the values were more than 70%, with no difference among the treatments, except for chlorpyrifos (Table 3).

Regarding the classification of parasitoid toxicity, the results indicate that the concentrations were within class 1 (innocuous) according to the IOBC classification, except for 50 g a.i. ha^-1 of chlorantraniliprole, which was classified as slightly harmful (class 2) (Table 4).

Parasitism capacity of T. podisi adults from pupae sprayed with chlorantraniliprole and chlorantraniliprole + lambda-cyhalothrin

The total number of parasitized eggs was significantly lower only in the chlorpyrifos treatment, where each non-sprayed female parasitized 0.5 E. heros eggs (Table 5). Females sprayed with chlorantraniliprole, chlorantraniliprole + lambda-cyhalothrin, and water parasitized between 79.20 eggs in the treatment with 20 g a.i. ha^-1 chlorantraniliprole to 106.6 eggs in the treatment with water (Table 5).

Significant differences occurred in the emergence of T. podisi only for the treatment with chlorpyrifos, with a percentage of 8.33%. The remaining treatments varied between 47.93% and 58.20% viability for chlorantraniliprole at 15 g a.i. ha^-1 and chlorantraniliprole + lambda-cyhalothrin at 30 + 15 g a.i. ha^-1, respectively, without significant differences (Table 5).

The sex ratio was shown to vary according to the product/concentration tested. There was emergence of 100% males in the treatment with chlorpyrifos and 86% in the mixture of chlorantraniliprole + lambda-cyhalothrin at 20 + 10 g a.i. ha^-1. For the other treatments, the sex ratio did not differ and had values between 0.36 for the mixture of chlorantraniliprole + lambda-cyhalothrin at 30 + 15 g a.i. ha^-1 to 0.66 for chlorantraniliprole at 50 g a.i. ha^-1 (Table 5).

The longevity of the parent females was lower for chlorpyrifos (1 day) and higher for water (19.55 days). Among the tested concentrations of chlorantraniliprole and chlorantraniliprole + lambda-cyhalothrin at 10 + 5 and 20 + 10 g a.i. ha^-1, there was no difference, with variations between 14.85 and 17.85 days for the treatments of chlorantraniliprole at 30 g a.i. ha^-1 and chlorantraniliprole + lambda-cyhalothrin at 10 + 5 g a.i. ha^-1, respectively. Females treated with the higher concentration mixture (30 + 10 g a.i. ha^-1) had a longevity of approximately 14.20 days (Table 5).

The lifetime parasitism decreased over the life of the females. For all treatments, peaks in parasitism occurred on the first and third day of egg exposure (Figures 1 and 2). The maximum amount of parasitized eggs per day was observed for the treatment containing chlorantraniliprole at 30 g a.i. ha^-1 (Figures 1 and 2). For the same treatment, a parasitism rate of 80% was reached between days 8 and 9. The other treatments ranged from the day 9 to 10, as well as having a lower number of parasitized eggs per day (1.2 eggs) on the day 15. For chlorpyrifos, due to the mortality rate of 100% of the parasitoids, it was not possible to assess parasitism capacity.

Selectivity of chlorantraniliprole and chlorantraniliprole + lambda-cyhalothrin to T. podisi adults

The percentage of parasitism varied among treatments in all periods tested and, at 24 hours, did not exceed 47%. The lowest level of parasitism occurred in the treatment with chlorpyrifos (1.27%), followed by the mixture of chlorantraniliprole + lambda-cyhalothrin at 30 + 15 g a.i. ha^-1 (15.12%), chlorantraniliprole + lambda-cyhalothrin at 20 + 10 g a.i. ha^-1 (28.45%), and chlorantraniliprole + lambda-cyhalothrin at 10 + 5 g a.i. ha^-1 (31.15%). Treatments with chlorantraniliprole, as well as with water, had similar percentages. 72 hours after contact between T. podisi adults and the respective products, the percentage of parasitism was similar in the concentrations of chlorantraniliprole and water, with values between 63.30% and 82.53% for chlorantraniliprole at 30 g a.i. ha^-1 and 10 g a.i. ha^-1, respectively. For the chlorantraniliprole + lambda-cyhalothrin mixtures at 10 + 5 g a.i. ha^-1 and 20 + 10 g a.i. ha^-1, parasitism was lower than for the other treatments, with percentages of 53% and 25.33%, respectively. For the highest concentration of the chlorantraniliprole + lambda-cyhalothrin mixture at 30 + 15 g a.i. ha^-1 and the positive control of chlorpyrifos, after 72 hours, there was no parasitism (Table 6). In the last assessment, 120 hours after adult contact with pesticides, parasitism did not differ between chlorantraniliprole and water, with values between 67.04% (30 g a.i. ha^-1 chlorantraniliprole) and 83.54% (10 g a.i. ha^-1 chlorantraniliprole). The mixture of chlorantraniliprole + lambda-cyhalothrin at 10 + 5 g a.i. ha^-1 showed the lowest percentage of parasitism (11.33%). For the mixtures with the highest doses, as well as the positive control with chlorpyrifos, there was no parasitism observed due to death of the parasitoids (Table 6).

Data on emergence differed only at 24 hours, when the lowest value observed was that of the treatment with chlorpyrifos (25%) and the highest values were for the mixture of chlorantraniliprole + lambda-cyhalothrin at 30 + 15 g a.i. ha^-1 (64.63%), chlorantraniliprole at 20 g a.i. ha^-1 (61%), chlorantraniliprole at 10 g a.i. ha^-1 (60%), and chlorantraniliprole + lambda-cyhalothrin at 10 + 5 g a.i. ha^-1 (58.17%). In the other treatments, the percentages of emergence were intermediate (Table 6).

Regarding the classification of toxicity of insecticides according to IOBC parameters, all the concentrations of chlorantraniliprole tested were not toxic to parasitoids at 24, 72, and 120 hours after contact with adult insects. The mixture of chlorantraniliprole + lambda-cyhalothrin 10 g a.i. + 5 ha^-1 was not toxic to the parasitoid 24 and 72 hours after contact with adult insects. These concentrations were classified as harmless (class 1) (Table 7). The mixture of chlorantraniliprole + lambda-cyhalothrin at 10 + 5 g a.i. ha^-1, 120 hours after contact with the parasitoids, caused an 86.31% reduction in parasitism of adults and was thus classified as moderately harmful (Table 7).

The highest concentrations of the mixtures - chlorantraniliprole + lambda-cyhalothrin at 20 + 10 g a.i. ha^-1 and 30 + 15 g a.i. ha^-1 - reduced parasitism after 24 hours to 31.23% and 63.44%, respectively. These concentrations were classified as somewhat noxious (Table 7). At 72 hours after contact with the parasitoids, the same mixtures reduced parasitism to 60.13% and 100%, respectively, and were considered slightly noxious at 20 + 10 g a.i. ha^-1 and noxious at 30 + 15 g a.i. ha^-1. After 120 hours, both reduced the parasitism of T. podisi by 100% and were classified as noxious (Table 7).

Spraying with chlorpyrifos was classified as moderately harmful 24 hours after contact with parasitoids, with a 96.92% reduction in parasitism (Table 7). For the other periods tested, 72 hours and 120 hours after contact, the reduction in parasitism was 100%, resulting in a classification of noxious to T. podisi adults (Table 7).

Discussion

Even with the reported toxicity of chlorantraniliprole in different doses to non-target organisms belonging to various groups, such as Daphnia magna (Crustacea) (LAVTIZAR et al., 2015) and to nymphs of Amphiareus constrictus (Stal) and Blaptostethus pallescens (Poppius) (Heteroptera: Anthocoridae) (GONTIJO et al., 2015), in general, this study found no significant influence of this product on the development of T. podisi. Accordingly, the product shows characteristics that allow us to consider it to be selective (LAHM et al., 2009; SPARKS et al., 2015). In addition, this molecule acts mainly on insects of the order Lepidoptera (IRAC, 2016), which may be related to its low degree of interference in the T. podisi parasitoid.

Thus, chlorantraniliprole has been classified as harmless to adult insects and pupae, except at the highest dose tested (50 g a.i. ha^-1). Similar results were observed for other species of egg parasitoids of the Trichogrammatidae family (PREETHA et al., 2009; BRUGGER et al., 2010; UMA et al., 2014) and for T. podisi in rice (PAZINI et al., 2016), where chlorantraniliprole was classified as innocuous at 31.5 g a.i. ha^-1. However, the highest dose of chlorantraniliprole still needs to be assessed in the field, where variables such as rain, wind, sunlight, and others minimize the action of the product on the organism. Additional studies are needed to address these factors.

In tests with Trichogramma galloi (Zucchi) (Hymenoptera: Trichogrammatidae), chlorantraniliprole led to a reduction in mortality of less than 30% and was classified as innocuous at 350 g a.i. ha^-1 (OLIVEIRA et al., 2013). For Trichogramma pretiosum pupae (Riley) (Hymenoptera: Trichogrammatidae), chlorantraniliprole was considered slightly harmful (BARROS, 2016), which in the present study occurred only with the highest dose of the product, in the first 24 hours of assessment for T. podisi. For adult insects, at all concentrations and periods tested, chlorantraniliprole was shown to be innocuous. Generally, the adult phase of the parasitoid is more sensitive to pesticides, compared to the pupal phase, which is considered more tolerant (CARMO et al., 2009). This is because the pupa is protected within the egg of the host during the pupal phase. The chorion of the host egg provides protection to the developing parasitoid, preventing the pesticide from reaching the parasitoid pupa inside the host (BUENO et al., 2017). However, the higher toxicity of chlorantraniliprole on pupae observed in this work can be explained by the penetration of the product through the chorion of host eggs due to their lipophilicity, thus leading to lack of viability of adult emergence (MACBEAN, 2012).

According to Brugger et al. (2010), there is no significant reduction in the emergence of T. pretiosum after application of chlorantraniliprole to H. armigera eggs. According to those authors, this insecticide can be viably used in IPM programs due to its selectivity with regard to non-target organisms, especially parasitoids. This result was also found in the present study. Thus, chlorantraniliprole-based products may allow for the concurrent use of biological and chemical control, with regard to the use of T. podisi.

In this study, the mixture of chlorantraniliprole + lambda-cyhalothrin significantly reduced the parasitism of T. podisi. Its negative effect intensified during the assessments, classified at 120 hours as harmful at the highest concentrations tested. According to Paiva (2016), the effect of the mixture of pyrethroid and neonicotinoid was also harmful to the T. pretiosum parasitoid. With the present results, decreased parasitism was also observed under the effect of chlorantraniliprole + lambda-cyhalothrin, demonstrating negative interference in the performance of the insect. This fact can be explained by the different modes of action of the insecticides, which together intensified their effect on parasitoid activity.

Regarding the parasitic capacity of the F₁ generation of T. podisi, neither chlorantraniliprole nor the mixture of chlorantraniliprole + lambda-cyhalothrin affected the total number of eggs that were parasitized, the viability of parasitism, or the sex ratio. This demonstrates that the spraying of various products and doses does not affect performance of the second generation of the parasitoid (sublethal effects).

In general, the adult phase of T. podisi was more sensitive to the products and doses applied. This pattern was also observed for other species of parasitoids (BUENO et al., 2008). Thus, the present study provides information for making choices about the insecticide to be used in pest management, favoring the integration of chemical and biological control, with the aim of better preserving natural enemies in agroecosystems.

Conclusion

Chlorantraniliprole was selective to T. podisi at the doses studied and can be considered a tool in IPM for soybeans, since it demonstrates low or null negative interference in the development of the parasitoid when sprayed on pupae and adults. However, the mixture of chlorantraniliprole + lambda-cyhalothrin should be used with caution in IPM, as it interferes negatively in the development of the parasitoid and should be substituted with a more selective product whenever possible.

Acknowledgements

The authors are grateful to Embrapa Soybean, the National Council for Scientific and Technological Development (CNPq) (processes 303779/2015-2 and 402797/2016-7) and the Coordination for the Improvement of Higher Education Personnel (CAPES) for granting financial aid and scholarships.

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Author notes

*Author for correspondence