Telenomus remus has been used as an efficient biocontrol agent in ABC programs of various species of the genus Spodoptera around the world (Pinto and Fernandes 2020, Ferrer 2021, Wengrat et al. 2021, Colmenarez et al. 2022, Laminou et al. 2023). Despite its efficiency as biocontrol agent in ABC of Spodoptera spp., the use of synthetic insecticides is still necessary in soybean and corn production, at least for a short and medium period of time (Burtet et al. 2017), making it necessary to ensure the compatibility of these control strategies to successfully apply IPM in those crops (Bueno et al. 2021, Bueno et al. 2023). Some authors have found that some insecticides from different chemical groups applied in these crops were selective for T. remus and therefore recommended their prioritization in IPM programs to preserve this parasitoid species (Bueno et al. 2008, Amaro et al. 2018, Bueno and Torres 2018, Mahjan and Bhamare, 2023).
In the present study, the insecticides evaluated for selectivity for T. remus showed differential toxicity, which may be related to various factors such as the developmental stage of the parasitoid, the characteristics of the host egg, and the physicochemical properties of the insecticides, such as lipophilicity and molecular weight (Bacci et al. 2006). The spray of the insecticide chlorpyrifos on eggs of S. frugiperda containing the parasitoid T. pretiosum in its immature stage reduced the emergence of parasitoids by 100%. This result is consistent with those described by Amaro et al. (2018) and Bueno et al. (2008), where chlorpyrifos reduced the emergence of T. remus when treated in the pupal stage inside host eggs. This insecticide belongs to the organophosphate chemical group and is reported in the literature as highly toxic to various species of pest arthropods as it acts on the insect's neurotransmitter system, preventing the enzyme acetylcholinesterase from deactivating acetylcholine and thus leading the insect to death due to hyperexcitability (Carmo et al. 2010).
The insecticides chlorantraniliprole, indoxacarb, and spinetoram, when applied to host eggs containing the parasitoid during the egg-larva and pupal stages, did not reduce the emergence of insects in the F1 generation and did not cause transgenerational effects, while chlorpyrifos was toxic. This difference in toxicity likely occurred because these products have different modes of action, distinct active ingredients, uncommon formulations, and belong to different chemical groups. Some insecticides may not be able to penetrate the chorion of S. frugiperda eggs and reach the parasitoid inside due to the structures of the host and parasitoid eggs (Potrich et al. 2017). The insect eggs consist of a nucleus, cytoplasm with yolk, a periplasm, and the chorion, the latter being formed by an outer layer, followed by an intermediate wax layer and then by the vitelline envelope. Furthermore, the chorion consists of two additional layers, the exochorion and the endochorion, both composed of 90% proteins (Chapman 1998; Klowden 2007; Potrich et al. 2017). Thus, the wax layer may have acted as a barrier to the entry of polar or very apolar insecticides. The lipophilicity of a product is determined by the octanol/water partition coefficient (log Kow). Chlorpyrifos has higher lipophilicity with log Kow 4.55 compared to other insecticides (Bentley et al. 2010, Sparks et al. 2012), which may have favored its entry into the egg and embryo intoxication. For this property, chlorpyrifos may also have had greater ease in crossing the lipid sublayer of the cuticle of the adult parasitoid and reaching its site of action, inhibiting acetylcholinesterase, as reported by Costa et al. (2014) for other insect species.
When comparing the effects of insecticides on the parasitoid during the egg-larva and pupal stages inside the host egg, no differences were found. These results corroborate the observations made by Gill et al. (2022) for the parasitoid Trichogramma chilonis Ishii, 1941. However, it is important to note that insecticides may have different responses depending on the developmental stage of the parasitoid (Croft 1990; Rodriguez-Saona et al. 2016).
The insecticides chlorantraniliprole, indoxacarb, and spinetoram did not negatively affect the sex ratio of the parasitoid when treated in its immature stage, while chlorantraniliprole and indoxacarb also did not influence this biological parameter of the offspring of treated adult females. Thus, it is expected that chlorantraniliprole and indoxacarb are compatible with the parasitoid and will allow its population growth and consequent greater control of pest insects in soybean and corn crops under field conditions.
For females that received direct application of the insecticides spinetoram and chlorpyrifos or were in contact with contaminated surfaces, mortality was 100%. Spinetoram is in the spinosyn group which functions as a stomach poison, with low activity of contact (Bret et al. 1997). In addition, spinosins are capable of promoting hyperexcitation of the nervous system by continuously activating the nicotinic acetylcholine receptors, resulting in involuntary muscle contractions and tremors, followed by paralysis and death of the insect (Drobnjaković 2023). Although sometimes classified as environmentally and toxicologically of reduced risk and usually less harmful to predators, hymenopteran parasitoids are significantly more susceptible to their effects (Williams et al. 2003). Previous studies have reported that spinetoram, when applied to adults of T. pretiosum, caused 100% mortality (Khan and Ruberson 2017). However, it is important to consider that the adult of these parasitoids is free-living stage and typically more sensitive to the action of pesticides compared to the immature stage, which is protected by the chorion of its host's egg (Potrich et al. 2017; Hassan 1992).
Application of chlorantraniliprole directly to adult females, caused reduction in parasitism compared to insects that were exposed to contaminated surfaces. This difference in the results is a consequence of the different application mode. When application is done directly to adults, some unvolunteered ingestion occurs, what does not happen when insects are exposed to the dry residue of pesticides on contaminated surfaces. The product acts mainly through ingestion and thus pose a low threat of direct contact exposure, they are quite selective, acting specifically on phytophagous insects, especially those of the order Lepidoptera, and can be considered safe for non-target organisms that do not feed on plants (Lahm et al. 2009). This result is consistent with that obtained by Mahajan and Bhamare (2023), who observed a decrease in parasitism when exposing adult T. remus to dry residues of chlorantraniliprole. However, other authors have reported that chlorantraniliprole has low toxicity to other species of parasitoids under laboratory conditions (Brugger et al. 2010, Silva et al. 2018). This insecticide acts on ryanodine receptors present in the sarcoplasmic reticulum membrane of the insect muscle cell and induces the release of Ca2+ ions into the cytosol, resulting in irreversible paralysis and consequent insect death (Nauen 2006, Ebbinghaus-Kintscher et al. 2007).
In both exposure routes, the insecticide indoxacarb reduced the percentages of parasitism of the F0 generation of the parasitoid T. remus. This insecticide belongs to the oxadiazine chemical group and acts as a sodium channel blocker in insect nerve cells, preventing the flow of sodium ions and inhibiting nerve impulse transmission, leading the insect to death (Wang et al. 2020). In the present study, although indoxacarb reduced parasitism and emergence of T. remus, it was classified as class 1 (harmless) by the IOBC classification, similar to the result of Liu et al. (2022), where this product was also considered harmless when applied to adults of Tetrastichus howardi (Olliff) (Hymenoptera: Eulophidae).
Taking into account that in laboratory selectivity studies the natural enemy is subjected to maximum exposure to the product, those that fall into classes 1 and 2 will also be compatible with T. remus under field conditions and can be used in IPM programs to preserve this parasitoid, while those in classes 3 and 4, such as chlorpyrifos, should be evaluated under field conditions to confirm their toxicity to the natural enemy or not.
It was observed that the insecticides chlorantraniliprole and indoxacarb showed low toxicity to T. remus and therefore are compatible with the parasitoid, and can be used in integrated pest management programs for S. frugiperda in soybean and corn crops.