Benzoates (naturally occurring plant toxins) produce pesticidal effects on various pest insects and mites, but their effects on non-target insects are poorly understood. In this study, we evaluate the lethal and sublethal toxicity of methyl benzoate (MB) to adults of the generalist predatory bug Nesidiocoris tenuis (Reuter) (Hemiptera: Miridae).To assess lethal effects, N. tenuis was exposed to plant surfaces treated with 0.25%, 0.5% and 1% MB, as well as negative and positive controls (water and the neonicotinoid acetamiprid, respectively). Exposure to 1% MB resulted in the highest corrected mortality of 17.8% and 13.3% under laboratory and greenhouse conditions, respectively. Thus, 1% MB can be classified as harmless to N. tenuis according to the International Organization for Biological Control rating scheme. At the sublethal level, MB exposure did not significantly affect the consumption of eggs of the whitefly Bemisia tabaci by N. tenuis relative to negative control feeding rates. In contrast, acetamiprid at the manufacturer’s recommended concentration reduced N. tenuis feeding activity by 45.4%. Furthermore, in a Y-tube olfactometer assay, there were no significant differences between the olfactory responses of N. tenuis to MB concentrations and the negative control (water). This study, therefore, suggests that MB could be used safely for pest control in combination with N. tenuis.
Integrated pest management (IPM) approaches, in which both biological and chemical control agents are applied against pests, are favored over pesticide-only approaches in sustainable production systems [1
]. However, the use of broad-spectrum chemicals in pest management can have negative effects on a target pest’s natural enemies and may impact the efficacy of these enemies as biological control agents [3
]. Therefore, further research into the adverse effects of pesticides on natural enemies is crucial for maintaining and improving the effectiveness of biological control systems and for evaluating the suitability of pesticides in IPM programs [1
]. Such research should assess the lethal and sublethal effects of chemical pesticides on natural enemies.
Lethal effects include any acute toxicity effects (i.e., mortality) of pesticides, whereas sublethal effects can be behavioral and/or physiological effects on individuals, including changes to their development, longevity, and/or reproduction [1
]. For the natural enemies of pest species, the risk assessment of pesticides is generally based on both lethal and sublethal effects. Traditionally, evaluation of pesticides for both registration purposes and compliance with IPM systems begins with an analysis of their acute toxicity, which provides fundamental data on the potential threat they pose to natural enemies [7
It is also important to consider various methods when evaluating the toxicity of pesticides to natural enemies, as well as the many potential routes of toxicant penetration into the animals’ bodies. Testing conditions could include any of the following: topical application used to replicate direct exposure of the natural enemies to spray droplets [8
]; residual toxicity studies, in which chemicals applied to plant surfaces or inert substrates replicate the interaction of natural enemies with crop residues [9
]; treated plants, in which pesticides in plant tissue contaminate plant resources, such as nectar or plant sap, that may be essential for the nutrition of natural enemies [10
]; and treated prey or hosts, since toxicants can transfer topically or by ingestion during predation or parasitism [11
]. The importance of these particular chemical entry routes depends on several factors, including the intrinsic properties of the pesticide and the biological and ecological characteristics of the particular natural enemy species.
The mirid bug Nesidiocoris tenuis
(Reuter) (Hemiptera: Miridae) is a generalist zoophytophagous predator of multiple pests that target tomato plants and other agricultural crops [12
]. N. tenuis
is mass-reared and released for crop protection in enhanced biocontrol programs designed to combat whiteflies and, most recently, the invasive moth Tuta absoluta
(Meyrick) (Lepidoptera: Gelechiidae) [15
]. Additionally, N. tenuis
also contributes to the control of thrips, mites, aphids, spider mites, leaf miners and some other lepidopteran pests in greenhouse and field environments [19
]. Thus, given the value of N. tenuis
as a biological control agent, it must become a focus of research on the lethal and sublethal effects of potential IPM pesticides.
The concurrent use of pesticides and alternative control agents is common in IPM programs. However, these combinations are not always compatible: some studies have demonstrated that predatory insects (i.e., natural enemies) can be more susceptible to chemical pesticides than the pests they prey upon [22
]. As potential alternatives to chemical pesticides in IPM, plant derivatives, including naturally occurring compounds such as essential oils, are typically safer for humans and the environment, and they may be more compatible with natural enemies, which themselves play crucial roles by reducing the risk of pest reappearance and the amount of pesticide used [25
]. Therefore, the impact of pesticides on natural enemies should always be considered when selecting chemical controls in IPM. Indeed, the use of selective pesticides, which affect insect pests, but are relatively harmless to natural enemies, will conserve natural enemies and thereby contribute to the success of IPM programs [26
In recent years, attempts have been made to develop pesticides of natural origin that are more environmentally friendly than synthetic pesticides [27
]. Benzyl methyl ester, also known as methyl benzoate (MB), is a volatile organic compound (often derived from fermented apple juice) found in many plant species [28
]. MB has recently been shown to have acute toxic effects on various insect species including whiteflies, aphids and mites [29
], which are the prey of N. tenuis
. Possible non-target effects of MB on natural enemies have yet to be fully investigated.
Here, the lethal and sublethal effects of MB on the important biological control agent N. tenuis were investigated. The ultimate goal of the present study was to enhance our knowledge of pest control methods suitable for IPM programs, and specifically to ensure that MB was safe for use with N. tenuis. Our results showed that the insecticidal toxicity of 1% MB could be classified as harmless to N. tenuis according to the International Organization for the Biological and Integrated Control of Noxious Animals and Plants, West Palearctic Regional Section.
2. Development and Finding
In the present study, exposure to dry residues of MB at 0.25%, 0.5% or 1% on tomato plant tissues did not significantly affect adults of N. tenuis
. Furthermore, exposures to these MB concentrations through topical spray or foraging on treated plant surfaces did not cause significant mortality or antifeedant effects. Indeed, in contrast to acetamiprid, MB did not reduce the feeding activity (consumption of eggs of B. tabaci
) of N. tenuis
which was comparable to that observed in the negative control. Although pesticides can interfere with the feeding behavior of exposed insects due to their repellent or antifeedant properties [1
], such effects were not observed for MB. In general, MB exposure resulted in <30% mortality of N. tenuis
, which corresponds to the harmless category in the IOBC toxicity classification.
MB is highly effective at 1% concentration when used against whitefly, aphid and mite pests: it can cause >70% mortality of these arthropods under laboratory and greenhouse conditions [30
]. In contrast, our present results indicate that 1% MB does not cause high mortality or adverse feeding effects on N. tenuis
. Differences in mortality between the insect pests and their predators may be due to differential susceptibility to the tested compound or differences in methods of treatment or differences in target stages of the tested organism. We suppose that herbivorous insects are susceptible, but omnivorous insects such as N. tenuis
are tolerable to MB. Likewise, Campolo et al. [43
] recently reported that the essential oil (EO)-based formulations of sweet orange were most toxic against the eggs and larvae of a specialist herbivorous insect pest, T. absoluta
, whereas least toxic towards the omnivorous predator N. tenuis
. Further studies are required to find the physiological or biochemical differences between the herbivorous and omnivorous insects after MB treatments.
MB at the concentration that harms whiteflies, aphids and mites can be regarded as relatively harmless to N. tenuis
. Similarly, Mostafiz et al. [31
] reported that the toxicity of 1% MB was very low in a study of the predatory lacewing Chrysoperla carnea
(Neuroptera: Chrysopidae). Thus, MB would appear to be a strong choice for use as a pesticide in combination with N. tenuis.
Other pesticides may also work well with N. tenuis.
Madbouni et al. [44
] also reported that the lethal and sublethal effects of pyriproxyfen and spirotetramat on N. tenuis
were minor (<30% mortality); therefore, these pesticides were considered harmless.
Natural enemies are likely to move between fields, crops and non-crop habitats, creating discontinuous exposure to pesticides. Some pesticides, such as neonicotinoids, not only cause neurotoxic symptoms, but also affect the behavioral parameters of predatory arthropods, e.g., orientation and/or foraging [1
]. The present study revealed that MB did not significantly affect the feeding rate of N. tenuis
. In IPM programs, it is important to consider both the lethal and sublethal effects of a chemical before attempting to use it for crop protection in conjunction with beneficial arthropod populations in order to maximize the natural enemies’ performance against pests. As well as consuming herbivorous insects, N. tenuis
can feed directly from plant tissues, honeydew and nectar [10
]. Thus, N. tenuis
could be exposed to pesticides by feeding on either prey organisms or treated plants. However, we showed that the tested MB concentrations did not harm N. tenuis
in a sublethal manner. Therefore, our findings indicate that MB is relatively harmless to N. tenuis
in in vitro
assays. Nevertheless, we propose that further testing is required, particularly under field conditions, in order to fully evaluate the effects of MB on these beneficial insects.
This is the first report on the possible lethal and sublethal effects of MB on the mirid bug N. tenuis that is used as a biological control agent. Given that the selection of a suitable insecticide in an IPM program not only depends on its efficacy against the target pest, but also on its toxicity to beneficial insects (as well as its degradation and persistence in the environment), the results of our laboratory and greenhouse experiments support the case for MB as an IPM pesticide. Indeed, we showed that MB is relatively harmless to N. tenuis. Future work on the sublethal and residual effects of MB, as well as long-term laboratory and field studies, will further advance our understanding of the impact of this naturally occurring plant toxin on N. tenuis and other non-target organisms.