It is crucial to consider a variety of aspects using well-established methodologies when classified the selectivity of insecticides to natural enemies (Bueno et al. 2017). Overall, taking the impact of different studied chemicals when sprayed over the pupae and adults of the parasitoids (T. podisi and T. teretis) and also over the E. heros eggs before parasitism, ethiprole was the most selective insecticide in this study, which can be classified as harmless (class 1) inside the pre-established IOBC categories (Hassan 1992). This higher selectivity is especially true for the lowest tested rate of 150 g/150 L H2O, which was slightly more selective than the chemical at the rate of 200 g/150 L H2O for some of the evaluated parameters. This dose-dependent side-effects of ethiprole had previously been reported for honeybee (Liu et al. 2021) but it is the first report for egg parasitoids.
Ethiprole is a new phenylpyrazole insecticide with structure analogue to fipronil. It is effective against a broad spectrum of sucking insects with pronounced plant systemic activity (Carboni et al. 2003), the reason why it has been widely used against stink bugs in soybeans. However, not only are stink bugs hard to be controlled but also harmful to soybean and maize plants severely reducing yield when not well managed (Gomes et al. 2020; Bueno et al. 2021) which has increased the use of insecticides and consequently pest resistance reports (Sosa-Gómez et al. 2001; Sosa-Gómez and Silva 2010). The insecticides used against stink bugs are restricted to a few different modes of action, worsening resistance issues with E. heros, which is the most frequent stink bug species occurring in the soybean field, especially in South America. Ethiprole is described as having some positive characteristics such as high level of selective toxicity (Simon-Delso et al. 2015) and thus cross resistance would be not likely. In particular, ethiprole binds to the gamma-aminobutyric acid receptor (GABAR) on the membrane of nervous system cells of the target organism, inhibiting the central nervous system of the insect (Cole et al. 1993; Garrood et al. 2015). This differs from the other modes of action available for stink bug control and then it is of crucial importance for insecticide resistance management. Being selective to the most important egg parasitoids of the pest is also another important positive feature that makes etriprole and important tool to stink bug manage in soybean and maize fields.
Despite its selectivity to the egg parasitoids T. podisi and T. teretis, it is important to emphasize the need of using ethiprole only, when necessary, which is when the economic threshold of 2 sting bugs/meter is reached or surpassed (Bueno et al. 2015). Telenomus podisi and T. teretis are only some of many species of beneficial organisms that should be preserved into the agroecosystem. Ethiprole has been observed to cause developmental deficiencies, disordered immune action, and abnormal reproduction and neurobehavior in some other nontarget organisms (Tanaka and Inomata 2017; Tanaka et al. 2018). Sublethal doses of ethiprole were reported to have physiologically toxic effects in honeybee larvae and adult honeybees inhibiting the pupation and eclosion rate of honeybee larvae (Liu et al. 2021).
Despite the taxonomic proximity of T. podisi and T. teretis, which belong to the same family (Scelionidae), the different results recorded between T. podisi and T. teretis when sprayed with the same insecticide and rate can have different reasons that should be studied in more details in future researches. Those variations in results are probably due to differences among the hosts species related to their size, chemical composition and thickness of cuticles among other reasons, for example. The greater the body volume of the beneficial organism, the smaller the specific area and, consequently, the lesser the exposure to insecticides (Picanço et al. 1997). Different insecticide penetration rates, related to physiological differences, chemical composition and thickness of T. poidsi and T. teretis cuticles might also help to explain the varying responses of those species to the studied insecticides (Fernandes et al. 2010). More hydrophobic insect cuticles result in higher affinity to insecticides, consequently, higher insecticide penetration and possibly higher insect mortality (Leite et al. 1998). Furthermore, insecticide selectivity might also be associated to ethion metabolization by cytochrome P450-dependent monooxygenase enzymes of beneficial organisms. These enzymes usually detoxify lipophilic compounds, converting them into metabolites and allowing natural enemies to eliminate toxic compound through their feces (Brattsten et al. 1986), a process which might differ between T. podisi and T. teretis.
Lambda-cyhalothrin is a pyrethroid that was tested mixed with a neonicotinoid (thiamethoxam) or a sulfoximine (sulphoxaflor) at different rates. Chemicals from the pyrethroid group act at sodium channels in the axon, causing hiperexcitation in the insects and killing them very quickly (Bueno et al. 2008). Treatment containing lambda-cyhalothrin triggered more severe negative side-effects to both T. podisi and T. teretis pupae and adults because this chemical is a neurotoxin that act similarly on the different species of insects, beneficials or pests, which share very similar nervous system. Thus, pyrethroids have a broad spectrum and are generally classified as non-selective for most beneficial arthropod species (Carmo et al. 2010). Various insecticides in this chemical group have been previously reported as harmful to different beneficial arthropods (Croft 1990; Croft and Whalon 1982; Sterk et al. 1999, Carvalho et al. 1999, Stecca et al. 2018). However, those negative side-effects can vary accordingly to the used chemical rate. Studied treatments containing lambda-cyhalothrin at higher rates (30 and 45 g/150 L H2O) were more noxious than treatments with lower rates of the pyrethroid (21.2 and 26.5 g/150 L H2O) to both parasitoid species. Furthermore it is important to note that both parasitoid species as pupae were more tolerant to the negative side-effects of insecticides when compared to adults. The higher tolerance of parasitoid pupae to chemicals had already reported in literature as a consequence of the protection offered by the chorion of the host egg to the parasitoid that develops inside its interior and is not reached by the sprayed chemicals (Stecca et al. 2016). This protection offer by the chorion of the host egg can vary accordingly to the insecticide because the ability of a chemical to penetrate the chorion of an insect egg may be related to their physicochemical properties. For example, chemicals with higher molecular weight have greater difficulty in crossing the chorion (Stock and Holloway 1993), which may explain the higher tolerance of T. podisi and T. teretis pupae inside host eggs to chemicals that are harmful to adults of the same species. However, this protection depends on how close the spraying occurs to adult parasitoid emergence. Pesticide residue that remains on the chorion of the eggs can be enough to kill wasps during emergence since those wasps use their mouthparts to cut the chorion during emergence, the moment they can get contaminated and die due to the insecticide. Then, despite not having the ability to penetrate the chorion, some chemicals with longer residual can still be able to kill natural enemies at the moment of adult emergence because of pesticide spraying that occurred on the pupae stage.
Thiamethoxam is a neonicotinoid which acts as a neurotoxin and interferes with the transmission of nerve impulses by binding to specific acetylcholine receptors (Talebi-Jahromi 2007). Sulfoxaflor is the first insecticide of the sulfoximine group (Zhu et al. 2011) acting on insect nicotinic acetylcholine receptors (nAChRs), but with a distinct combination of attributes from the neoniotinioids (Sparks et al. 2013). Both thiamethoxam and sulphoxaflor were only tested in mixture with the pyrethroid as recommended in the field to manage stink bugs. Therefore, it does not allow to make further insides about their selectivity on this study. However, both neonicotinoids, sulfoximines and as already mentioned also pyrethroids are reported as harmful to most natural enemies (Tomizawa and Casida 2005; Jiang et al. 2019). The main difference among those chemical groups is that pyrethroids have a contact action, which facilitates the exposure and action of this insecticide to parasitoids and other beneficial organisms in the field. On the other hand, neonicotinoids and sulfoximines are systemic products with little contact action. These insecticides need to be ingested by insects and, therefore, are more specific against phytophagous sucking insects that, due to their feeding habits, come into contact with the product when they feed on the sap and/or nectar of plants, which is the case with parasitoids of T. podisi and T. teretis (Santos et al. 2006). Therefore, sulfoxaflor possess similar adverse effects on parasitoid wasps like neonicotinoids as reported for the egg parasitoids Trichogramma dendrolimi (Matsumura, 1926), Trichogramma ostriniae (Pang and Chen, 1974) and Trichogramma confusum (Viggiani, 1976) (Hymenoptera: Trichogrammatidae) (Jiang et al. 2019).
Chorpyrifos is an organophosphate that kill insects primarily by phosphorylation of the acetylcholinesterase enzyme (AChE) at the nerve endings. This type of poisoning causes loss of the available AChE and over-stimulation of organs by excess acetylcholine at the nerve endings and affects beneficial and pest insects similarly. Therefore, like pyrethroids, sulfoximine and neonicotinoids tested in this study, organophosphates are generally harmful to all insect groups. Noxious results of organophosphates on beneficial arthropods have been reported in the literature for T. pretiosum (Bueno et al. 2008) and T. cacoeciae (Hassan et al. 1988).
Among the tested insecticides used to manage stink bug outbreaks, the mixture of neonicotinoids + pyrethroids and the organophosphates are among the cheapest insect-control products available to farmers, what can lead to a overuse of those chemicals. However, their application is not compatible with the preservation of the most important stink bug biological control agents, the egg parasitoids from the Scelionidae family, as shown in this work. Therefore, those chemicals should be used with caution, always adopting the stink bug economic thresholds and whenever possible replaced, by less harmful products in IPM programs. Good alternatives to those products, when feasible, is the ethiprole, since their effects on T. podisi and T. teretis are less injurious as shown in this work.
It is important to emphasize that these experiments were carried out under controlled environmental conditions in the laboratory, where parasitoids were subjected to the highest possible pressure from the pesticides. Under field conditions, however, the negative impact of some of the tested pesticides may be reduced, since T. podisi and T. teretis can benefit from refuge areas or may avoid chemical-treated areas (Hassan 1992, Carmo et al. 2010).