Plants produce secondary metabolites to protect themselves against herbivores and pathogens (Levin, 1976; Rhoades and Cates, 1976; Mithöfer and Boland, 2012). These secondary plant metabolites may be constantly present within the plant (constitutive defenses) or they may be produced in response to attack by an herbivore or pathogen (induced defenses) (Karban and Myers, 1989). Induced defenses rely on signaling compounds known as ‘elicitors’ to initiate the plant’s defense response pathways. Elicitors include a wide variety of molecules, such as proteins, lipids, and carbohydrates found in various plant, microbial, and insect products (Lyon, 2007; Reignault and Walters, 2007; Meena et al., 2022). Once a plant interacts with an elicitor, one or more signal-transduction pathways are activated. Two important signal-transduction pathways involved in plant defenses are regulated by the phytohormones jasmonic acid (JA) and salicylic acid (SA) (Karban and Baldwin, 1997; Smith et al., 2009; War et al., 2012). The JA-mediated pathway is typically induced in response to chewing damage or necrotrophic pathogens (Walling, 2000; Beckers and Spoel, 2006). In contrast, the SA-mediated pathway is associated with immune responses to piercing-sucking insects (War et al., 2011) or biotrophic pathogen infection (Thomma et al., 1998; Glazebrook, 2005).

Recently, there has been significant interest in the potential of exogenously applying naturally found elicitors or their synthetic derivatives to protect plants against herbivores and pathogens (Ruiz-García and Gómez-Plaza, 2013; Bektas and Eulgem, 2015; Moreno-Pérez et al., 2020). Several elicitors of the SA pathway are commercially available as ‘plant bioactivators’ of defenses and are often marketed as biofungicides (Bektas and Eulgem, 2015; Zehra et al., 2021). These synthetic elicitors have been successful at increasing resistance to pathogenic diseases in many crops, such as Pythium damping-off in cucumbers (Benhamou and Bélanger, 1998), powdery mildew in okra (Vimala and Suriachandraselvan, 2008), and fire blight in apples (Brisset et al., 2000). A few studies have also reported reductions in the fitness of herbivorous arthropods that fed on crops treated with an elicitor (Correa et al., 2005; Uefune et al., 2014; Gordy et al., 2015; Sobhy et al., 2015). For example, the application of the SA-elicitor Actigard to potted pear trees reduced the survival of the pear psylla Cacopsylla pyricola (Förster) under laboratory conditions (Cooper and Horton, 2015), but failed to provide sufficient protection under field conditions (Cooper and Horton, 2017). Thus, by inducing host-plant resistance, elicitors of plant defenses may hold promise as environmentally safer alternatives to conventional insecticides employed in pest management programs (Stout et al., 2002; Pickett et al., 2014; Bektas and Eulgem, 2015; Divekar et al., 2022); however, additional studies are required to assess their efficacy under both laboratory and field conditions.

The vinegar fly spotted-wing drosophila, Drosophila suzukii (Matsumura) (Diptera: Drosophilidae), is an invasive pest from Southeast Asia that causes severe damage to soft, thin-skinned fruits such as raspberries, strawberries, and blueberries (Walsh et al., 2011; Lee et al., 2015). While other control methods, such as cultural control, behavioral control, and biological control, are currently under evaluation (Lee et al., 2019; Tait et al., 2021), D. suzukii management continues to depend heavily on frequent insecticide sprays (Diepenbrock et al., 2016). However, due to the unsustainability of continued insecticide use, behavioral manipulation may be more sustainable for D. suzukii management. Adults of D. suzukii utilize several cues from ripe host fruits and symbiotic microbes to detect suitable sites for feeding, mating, and oviposition (Keesey et al., 2015; Cloonan et al., 2018). One potential way of changing these cues is by applying elicitors of plant defenses to fruit crops. Elicitors may directly induce changes in the quality or quantity of volatiles typically emitted from fruits (Pagadala Damodaram et al., 2015; Salifu et al., 2022) or indirectly through their fungicidal effects on associated microbes. For instance, elicitors of the SA pathway may reduce the presence of Hanseniaspora uvarum, a symbiotic yeast closely associated with D. suzukii (Hamby et al., 2012), and thus reduce the attractiveness of fruits to flies (Hamby and Becher, 2016; Rehermann et al., 2022). In fact, fungicides have successfully reduced H. uvarum levels in other fruits, such as grapes (Agarbati et al., 2019). However, the effects of commercially-available elicitors of plant defenses on D. suzukii behavior towards fruits have not yet been studied.

Here, we hypothesized that elicitor-induced responses in fruits may cause D. suzukii adults to avoid these fruits or reduce the performance of larvae within the fruits. To test this hypothesis, we treated highbush blueberries, Vaccinium corymbosum L., fruits exogenously with four elicitors – three that primarily activate SA-related plant defenses (Actigard, LifeGard, and Regalia) and one activator of JA-related defenses (Blush) – to determine their effects on D. suzukii preference and performance. This was achieved through a series of no-choice and choice experiments conducted under laboratory, semi-field, and field conditions. Because Van Timmeren et al. (2020) successfully inhibited H. uvarum growth in the laboratory with a crop sterilant (peroxyacetic acid and hydrogen peroxide) developed for disease control, we also included a crop sterilant (OxiDate) in our study. The findings from our study may contribute to the potential behavior-based management options currently available for D. suzukii.

In this study, four elicitors and a crop sterilant were assessed as potential behavior-modifying products for D. suzukii management under the hypothesis that they would induce changes in the fruit, either directly or indirectly by influencing associated microbes, making them less attractive to this pest. However, our findings showed inconsistent repellency or oviposition deterrent effects of these products, posing challenges in drawing definitive conclusions regarding their long-lasting effectiveness under field conditions. While Actigard reduced D. suzukii oviposition in berries at 1 DAT in both no-choice and choice tests, its effect was short-lived; thus, it would necessitate multiple sprays within a week to make it effective, which may be impractical as a control option. In some cases, flies were even more attracted to the treated berries. For instance, although the specific mechanism(s) remain unknown, Regalia-treated berries were more attractive to the flies at 1 DAT and 7 DAT, and more flies chose LifeGard-treated berries at 10 DAT. Furthermore, none of the tested products showed significant larval toxicity effects, as evidenced by the similar correlation between egg counts and adult emergence across most assays. This suggests that these products, while not consistently, could potentially influence adult behaviors such as attraction and oviposition under certain circumstances.

While the elicitors and sterilant treatments used in our study did not consistently produce the expected repellent or oviposition deterrent effects on D. suzukii, products similar to those employed here effectively enhanced plant resistance against other insect pests. For example, various studies have demonstrated that application of SA induces defenses in plants, leading to reduced feeding (Stella de Freitas et al., 2019; Wei et al., 2021) and oviposition (Shahabinejad et al., 2014) by insect herbivores. However, most of these studies focused on folivorous insects, unlike our study, which examined a frugivore. An exception is the study by Damodaram et al. (2015), where the application of acibenzolar-S-methyl, the active ingredient in Actigard, to mangoes resulted in increased levels of phenols and flavonoids in the fruits. This, in turn, led to reduced oviposition, larval performance, and adult emergence of the oriental fruit fly Bactrocera dorsalis (Hendel). Recently, Hussain et al. (2023) also reported an increase in the levels of phenols, tannin, and flavonoid content and a decrease in the number of eggs laid by D. suzukii females in wine grapes treated with JA and SA. In addition, they found that SA-treated diet reduced D. suzukii oviposition in a dose-dependent manner. Among all the elicitor and sterilant treatments we employed, the SA-related Actigard demonstrated in some assays repellency and oviposition deterrent effects on D. suzukii when applied to blueberry fruits; however, the underlying mechanism(s) behind these effects remain unexplored. Like the findings by Hussain et al. (2023), Actigard also exhibited a reduction in egg laying in choice tests when applied to the diet. Thus, it remains unclear to what extent the observed effects of Actigard on D. suzukii resulted from directly influencing adult behavior or indirectly through alterations in fruit chemistry.

Van Timmeren et al. (2020) conducted studies using the crop sterilant Jet-Ag, whose active ingredients are the same as OxiDate, and found that it does not reduce D. suzukii oviposition in treated berries; however, it reduced the number of larvae infesting the berries. When directly applied to H. uvarum colonies in the laboratory, the sterilant inhibited yeast growth in a dose-dependent manner (Van Timmeren et al., 2020). In our study, the crop sterilant OxiDate did not elicit strong aversion from the flies or reduce fruit infestation. It is possible that, under field conditions, applying a crop sterilant to blueberries does not provide sufficient coverage to inhibit H. uvarum growth. Van Timmeren et al. (2020) also noted that Jet-Ag breaks down quickly under field conditions, resulting in limited residual activity. Moreover, recent research by Schöneberg et al. (2024) revealed that, under high pest pressure, Jet-Ag does not offer adequate standalone control against D. suzukii under field conditions, even when it occasionally reduced fruit yeast levels. Given these current findings, incorporating elicitors of plant defenses or crop sterilants as a standalone control option for D. suzukii may be challenging.

Our earlier studies revealed that Blush, an elicitor of JA-related defenses, has either no or minimal activity on D. suzukii and was consequently excluded as a treatment in subsequent studies. Initially, we included Blush based on findings from prior research suggesting that applications of JA could be effective for crop protection against insect herbivores (Uefune et al., 2014; Wei et al., 2021). However, these earlier studies primarily focused on foliar feeders, leaving the effects of JA and related elicitors of the JA pathway on frugivores unclear. Several studies have shown that applications of JA increase volatile emissions in plants that attract natural enemies and thus could enhance biological control of crop pests (Lou et al., 2005; Bruinsma et al., 2009). Consequently, applications of JA elicitors may have positive impacts on natural enemies of D. suzukii, such as the larval parasitoids Ganaspis brasiliensis (Ihering) and Leptopilina japonica (Novković and Kimura) (Wang et al., 2018), by enhancing their attraction to infested berries. It is also possible that SA and JA elicitors might reduce D. suzukii larval developmental times, a parameter not measured in our study, rendering them more susceptible to parasitism as stated by the ‘slow-growth high-mortality’ hypothesis (Feeny, 1976; Benrey and Denno, 1997). Indeed, reductions in development times were observed in stinkbug, Oebalus pugnax (F.), nymphs that fed on SA-induced plants (Stella de Freitas et al., 2019) and larvae of the fall armyworm, Spodoptera frugiperda (J. E. Smith), that fed on JA-induced plants (Gordy et al., 2015). Future studies examining elicitor treatments within the context of tri-trophic interactions could yield valuable insights for enhancing biological control efforts against D. suzukii.

Numerous abiotic and biotic factors, including environment, plant nutrition, genotype, and baseline resistance levels, can influence induced resistance in plants (Walters and Fountaine, 2009). Consequently, achieving efficacy in utilizing plant defense elicitors and crop sterilants in the field can be challenging. In our field cage experiments, nearly all D. suzukii adults emerged from fruits collected from the lower parts of the bushes. This observation aligns with previously reported D. suzukii adult behaviors, which prefer to target berries closer to the ground and within the interior of bushes, benefiting from cooler temperatures and higher humidity (Rice et al., 2017). It is conceivable that certain areas of the bushes were not thoroughly sprayed, potentially hindering the induction of a strong defense response. Weather conditions could have also influenced our field results. Notably, rain was experienced on the morning of the third day after treatment for replicates 1 and 2, which could have diminished the residual activity of the treatments. Future experiments should also consider the timing of the elicitor/sterilant treatments. In our study, non-infested berries were treated only once and when they were already ripe. Investigating whether it might be more effective to treat them before ripening and continuously thereafter is warranted. For instance, exposure to the elicitors or sterilants before ripening could potentially induce a more rapid increase in defenses after oviposition or larval feeding, a phenomenon referred to as ‘priming’ (Goellner and Conrath, 2008). It is also possible that these products could have ovicidal or larvicidal effects on D. suzukii post-infestation, as evidenced by the curative activity of some insecticides (Wise et al., 2015).

While this study did not find strong evidence supporting the use of the tested elicitors of the SA and JA defense pathways or crop sterilants as effective long-lasting behavior modifiers for D. suzukii in blueberries, these or similar products may still find utility in managing this pest for other purposes. For instance, although we cannot recommend them as standalone tools in a D. suzukii management program, future research could explore alternative applications, such as enhancing biological control or incorporating them into trap cropping or push-pull systems. Furthermore, it is plausible that elicitors may show greater efficacy against D. suzukii in other crop systems. Host-plant resistance remains a relatively unexplored tool for D. suzukii management, and multiple interacting factors can influence how a plant responds to elicitors of defenses or crop sterilants. With further refinement through future studies, there is potential to integrate induced host-plant resistance into D. suzukii management programs, offering a safer and more sustainable approach to protect crops against this invasive pest.

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

The manuscript presents research on animals that do not require ethical approval for their study.

AQ: Conceptualization, Data curation, Formal Analysis, Methodology, Writing – original draft. PU-B: Conceptualization, Data curation, Formal Analysis, Methodology, Writing – review & editing. RH: Methodology, Writing – review & editing. CR-S: Conceptualization, Funding acquisition, Resources, Supervision, Validation, Writing – review & editing.