The cabbage seedpod weevil (Ceutorhynchus obstrictus Marsham) is widely distributed and one of the most important oilseed rape pests in Europe (Williams, 2010) and North America (Buntin, 1998; Dosdall et al., 2006; Dosdall and Mason, 2010). Adult C. obstrictus feeds on flower buds and young pods of oilseed rape plants, but the main economic loss is caused by larvae feeding within the seedpods (Bonnemaison, 1957; Williams and Free, 1978). Management of C. obstrictus is mostly based on synthetic insecticides that have harmful effects on biodiversity, pollute the environment (Geiger et al., 2010) and may leave pesticide residues on products (Yigit and Velioglu, 2020). Broad-spectrum insecticides have fatal effects on naturally occurring predatory arthropods such as lacewings, spiders, ladybirds, carabid beetles, rove beetles and parasitoids, which otherwise can effectively control the abundance of agricultural pests and reduce the need to apply insecticides (Tschumi et al., 2016; Begg et al., 2017; Albrecht et al., 2020). For example, key parasitoids of C. obstrictus can substantially contribute to biocontrol services, as the parasitism rate of C. obstrictus can reach up to 90% (Veromann et al., 2011; Kovács et al., 2019). In the light of the European Union’s Farm to Fork Strategy which aims to diminish the negative impacts of agriculture on the environment, there is a great need to find environmentally sustainable pest control measures (European Commission, 2020).

Essential oils are of interest in pest science, as a possible alternative to synthetic plant protection products (Menossi et al., 2021; Devrnja et al., 2022). Several studies have highlighted their insecticidal effects on important agricultural pests (Das et al., 2021; Devrnja et al., 2022). An added complexity of essential oil studies is due to the variable chemical composition, even within the same plant species, as a result of different cultivars, growing conditions, production methods, plant parts used and harvesting times (Figueiredo et al., 2008; Baser and Buchbauer, 2009; Turek and Stintzing, 2013). Previously, several studies have examined the potential of essential oils to control another oilseed rape pest – pollen beetle (Brassicogethes aeneus Fabricius) (Mauchline et al., 2005; Pavela, 2011; Mauchline et al., 2013; Dorn et al., 2014; Willow et al., 2020). Pavela (2011) found that Carum carvi L., Thymus vulgare L. and Foeniculum vulgare Miller had an insecticidal effect against the pollen beetle, while Willow et al. (2020) showed only a slight insecticidal effect of residual exposure using very high dosage of Cinnamomum verum J. Presl oil; Mauchline et al. (2005); Mauchline et al. (2013) and Dorn et al. (2014) found repellent and lethal efficacy with Lavandula angustifolia Miller while Cook et al. (2007a) indicated no behavioural response from the main parasitoids Phradis interstitialis Thomson and P. morionellus Holmgren. However, it is unknown whether these essential oils are effective against another oilseed rape pest, C. obstrictus, as well which could potentially aid in the control of these two major pests simultaneously. While botanical insecticides are considered to be less toxic to humans and the environment compared to synthetic pesticides, their impact on the natural enemies of pests should be assessed, as they can interfere with their behavior or biology (Rampelotti-Ferreira et al., 2017; Parreira et al., 2018; Lima et al., 2020; Stenger et al., 2021).

Biosafety of plant protection products is a major concern in agriculture. Ideally, plant protection product applications should not be at the expense of non-target organism populations, especially those contributing to biological control of the target pest. Some essential oils have been evidenced as safe for such beneficial insects. For instance, essential oil residues of Origanum vulgare L. and T. vulgaris showed no sublethal or lethal effects in the parasitoid Trissolcus basalis Wollaston (Platygastridae) in direct contact and fumigation bioassays (Werdin González et al., 2013). Essential oil from Piper aduncum L. showed promising results to control the stink bug Euschistus heros Fabricius, while parasitism and emergence of the egg parasitoids Telenomus podisi Ashmead (Platygastridae) and Trissolcus urichi Crawford (Scelionidae) were unaffected (Turchen et al., 2016). However, decreases in parasitism rate have been observed in other species (Boeke et al., 2003; Stenger et al., 2021), leaving the biosafety profile of essential oils questionable with regard to parasitoids.

In this study, we aimed to investigate whether the dry residues of six plant essential oils affect the mortality and immobility of C. obstrictus, as well as mortality and immobility, and next generation development of the model parasitoid Nasonia vitripennis Walker (Hymenoptera: Pteromalidae). We show that Cuminum cyminum L. and C. verum essential oils have potential for use in C. obstrictus management, but also that their impact on parasitoids needs further study to determine the actual potential of these essential oils within integrated oilseed rape protection.

The present study showed that contact with essential oil residues via treated oilseed rape leaves and flowers caused both mortality and immobility in C. obstrictus adults. In addition to C. obstrictus, essential oil treatments showed an impact on the mortality and immobility of a model pteromalid parasitoid, N. vitripennis, and furthermore influenced the number of next generation adult parasitoids that emerged from their hosts. Our results showed that at 24 h post-treatment with C. cyminum and C. verum essential oils at 1.5% concentration they were as effective as the synthetic insecticide lambda-cyhalothrin, mortality and immobility of C. obstrictus adults reached 82.5% for C. verum and 50.7% for C. cyminum. There is an overlap in the occurrence of B. aeneus and C. obstrictus in oilseed rape fields (Veromann et al., 2006; Sulg et al., Under Review); B. aeneus arrives a little bit earlier than C. obstrictus, as its flight threshold temperature is 12°C (Williams, 2010), whereas for C. obstrictus, it is 13–15°C (Free and Williams, 1979; Lerin, 1991). However, they are both present in oilseed rape fields from the green bud stage (BBCH 51) (Veromann et al., 2006; Veromann et al., 2012). Therefore, it is possible that treatments targeting B. aeneus may also contribute to C. obstrictus control and vice versa. Our new findings show the potential of C. verum essential oil to manage C. obstrictus, but as it greatly exceeds that of previously reported for B. aeneus (17.5% combined immobility and mortality) (Willow et al., 2020), the two species are unlikely to be managed simultaneously using only C. verum. Based on previous results and our new findings, the treatment of oilseed rape with C. verum affects two of its main pests to some extent, therefore indicating the need for further investigations. The essential oils used in our study were almost the same (excluding anise) as in Willow et al. (2020). Gas chromatography–mass spectrometry results of the C. verum oil used in the present study are reported in detail in Willow et al. (2020). The primary active compound in the C. verum oil used was reported to be (E)-cinnamaldehyde (46%), followed by caryphyllene (15%), linalool (12%) and D-limonene (8%).

According to our best knowledge, the toxicities of essential oils for C. obstrictus, or other species in the genus Ceutorhynchus, have not previously been assessed. However, there are previous studies examining other members of the family Curculionidae, where essential oil treatment efficiencies have been examined. For instance, essential oils isolated by hydrodistilling the dried fruit of Trachyspermum ammi (L.) Sprague ex Turrill (Apicaceae) and Nigella sativa L. (Ranunculaceae) have shown repellent activity and toxic effects against the rice weevil (Sitophilus oryzae L.) (Chaubey, 2012). The rice weevil was also examined by Saad et al. (2018), where they found that, from all examined compounds contributing to acetylcholinesterase inhibition, the most promising was trans-cinnamaldehyde. Different essential oils, including C. verum, were studied against the stored product pest Sitophilus zeamais Motschulsky by Ramlal et al. (2020). They observed repellent and lethal effects of C. verum oil, resulting in 78% and 97% mortality at concentrations of 75 and 100 µL/mL, respectively. Similar to our study, the main constituent of C. verum essential oil in their study was cinnamaldehyde (62%) confirming that this compound can be potentially exploited against weevil pests.

The mortality rates in other essential oil treatments in our study were under 50% at 24 h, suggesting that their efficacy was insufficient for use in controlling C. obstrictus abundance in oilseed rape crops. In the present study, we did not examine other effects than mortality and immobility of these essential oils on C. obstrictus adults, e.g. repellence etc. For instance, previous studies have shown the repellent effects of essential oils on insects (reviewed in Lee (2018)) and also their potential to be used in storage facilities as pest management approaches (Cook et al., 2007b; Nerio et al., 2010; Campolo et al., 2018; Xu et al., 2018; Bandeira et al., 2021), but the use for managing agricultural pests have gained less attention. Essential oils can also be used to manage agricultural pests, but in order to use them in agricultural fields, the essential oils need to be more stable, preventing them from evaporating or biodegrading (Oladipupo et al., 2022). Future studies on C. obstrictus should examine behavioral effects in addition to the effects examined in the present study as exposure to essential oils, as well as treatment residuals, can result in behavioral changes, for example deterring egg laying or acting as antifeedant (Lazarević et al., 2020; Magierowicz et al., 2020; Stenger et al., 2021). Examining our two most effective (against C. obstrictus) essential oils, C. verum and C. cyminum, at four different concentrations, showed C. verum oil at 1% concentration to be the most efficient, resulting in almost 90% mortality and immobility at 24 h post-exposure, whereas C. cyminum oil at 2% concentration resulted in 90% morality and immobility at 24 h post-exposure. We presented mortality and immobility rates, since in nature, immobility is likely to result in mortality. Immobile insects are easier prey, as well as they may also die of dehydration, starvation, cold or heat stress, etc., as a result of being in contact with toxic substances.

Similar to other insecticides, the effects of essential oils on non-target organisms, including economically beneficial insects, should always be assessed. It is necessary to assess the impact of essential oils on the natural enemies of target pest species (e.g. relevant model parasitoids). The present study demonstrated that C. verum essential oil has the potential to control abundance of C. obstrictus, but at the same time it resulted in almost 100% mortality in the model pteromalid parasitoid N. vitripennis at 3 h post-exposure to treatments at 1.5% concentration of all studied essential oils except C. sativa. Testing the oils at 0.1% concentration showed that at 3 h post-exposure, T. vulgaris oil residues resulted in the highest mortality and immobility rates in N. vitripennis, although some parasitoids were able to recover from immobility by the 24 h time point. Similar to our results, Werdin González et al. (2013) found that one day old residues of T. vulgaris essential oil resulted in 100% mortality in parasitoid Trissolcus basalis Wollaston (Platygastridae) while one week old residues did not result in any mortality. When targeting a pest species, knowledge of parasitoid distribution in or arrival to the crop is crucial, as pesticide application times can be planned in a manner where the pesticide residues represent an insignificant threat to target pest-relevant biocontrol agents. Essential oil residues of C. verum show promising results for controlling C. obstrictus. However, C. verum oil treatment, at 0.1% concentration, resulted in an immobility rate of 17% in N. vitripennis. Increasing the concentration of C. verum oil to 0.3% resulted in almost four times this immobility rate in N. vitripennis, and residues from a 0.5% concentration application of C. verum oil resulted in 100% immobility. Thus, residues of C. verum essential oil, even when applied in low concentrations, are not safe for the parasitoid N. vitripennis. It remains unclear whether the essential oils could cause side effects in the next generation of N. vitripennis.

When treating parasitized pupae with C. sativa and C. cyminum it lowered hatching of the new generation of N. vitripennis to the same level as treatment with insecticide. But as direct exposure to essential oil residues, in the concentration of 1.5%, caused 100% mortality after 3 h among N. vitripennis, we can only assume that fly pupae served as protective shield mitigating the toxic effect of treatments. It has been reported that lambda-cyhalothrin can alter the ability of the parasitoids to find and infest their hosts, even when mortality is not observed among next generation female parasitoids (Desneux et al., 2004). Even though parasitoids developed in our study, their following parasitism efficacy remains unknown, and should be investigated in future studies. Whether the pods concealing parasitoids of C. obstrictus provide similar protection from developing parasitoids needs investigating. It also remains unknown whether the essential oil treatments in the present study had sublethal effects on next generation adult parasitoids, representing a crucial knowledge gap that is in need of assessment. Undetected sublethal effects, could result in death or decreased fecundity or jeopardize host location abilities. Our results show the potential of essential oils use in controlling C. obstrictus. However, much more research is needed before essential oils could be recommended for pest control.

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

SS, RK, and EV conceived the study. SS, TK, and RK performed the experiments. SS performed data analyses and visualization. SS and EV wrote the first draft of the manuscript. All authors contributed to the article and approved the submitted version.