Knowledge of the distribution and abundance of resident parasitoid species of Drosophila flies constitutes an important base for developing and implementing a biological control program for Drosophila suzukii (Matsumura) (Diptera: Drosophilidae), an invasive pest that attacks ripening thin-skinned wild and cultivated berries and stone fruits. For this purpose, a field survey was conducted to identify the parasitoid community associated with D. suzukii infested sites in tart cherry orchards and woodlots in west, northwest, and central Michigan. Sentinel traps baited with D. suzukii larvae and pupae in banana slices were deployed in the center of tart cherry orchards, in woodlots adjacent to tart cherry orchards, and in woodlots isolated from any known commercial host of D. suzukii. Traps were placed from the beginning of July to the end of October 2021. Three parasitoid species that are known to use drosophilids as hosts were recovered from these traps. Pachycrepoideus vindemiae (Rondani) (Hymenoptera: Pteromalidae) and Leptopilina boulardi Barbotin, Carton & Keiner-Pillault (Hymenoptera: Figitidae) emerged from the infested bananas. Leptopilina heterotoma (Thomson) was collected as an adult in a sentinel trap. Among these wasps, only P. vindemiae successfully parasitized D. suzukii pupae in the laboratory. This pupal parasitoid was abundant and widely distributed in both cherry orchards and woodlots. The highest number of P. vindemiae was collected from orchards, followed by woodlots adjacent to orchards, with woodlots without nearby cultivated fruit having the lowest detections. These findings suggest that future release of augmentative or classical biological control agents for D. suzukii could be successful in orchards post-harvest to control late-season populations of this pest.

biological control, sentinel trap, spotted wing drosophila, wasp

Since its first detection in Michigan in 2010, spotted-wing Drosophila, Drosophila suzukii Matsumura (Diptera: Drosophilidae), has rapidly become the number one pest of small fruits and cherries in Michigan. Due to a zero tolerance for detectable larvae in these fruits, growers have relied almost entirely on calendar-based spray programs to protect their valuable crops from D. suzukii damage prior to harvest (Van Timmeren and Issacs 2013). These intensive spray programs target the adult flies but have also disrupted existing IPM programs developed for other insect pests, with potential cascading effects on the environment, especially non-target organisms (Tait et al. 2021). Moreover, these high-input control strategies are costly for growers, particularly those that are growing processing fruits with a lower profit margin such as tart cherry. All these factors have motivated researchers to search for effective and environmentally sustainable long-term solutions to prevent crop damage by D. suzukii.

Biological control is a vital component of an IPM strategy of invasive insect pests (Lee et al. 2019) and remained unutilized in the framework of D. suzukii management until recently (Gabarra et al. 2015; Woltz et al. 2015). Explorations for potential classical biological control agents in Japan, South Korea, and China, where D. suzukii is native or endemic, found three dominant larval parasitoids that predominately attack D. suzukii: Asobara japonica Belokobylskij (Hymenoptera: Braconidae), Ganaspis brasiliensis (Ihering) and Leptopilina japonica Novkovic & Kimura (Hymenoptera: Figitidae) (Wang et al. 2020a). In addition, over 50 frugivorous drosophila parasitoids have been reported worldwide, and several common larval drosophila parasitoids in the Americas and Europe have been evaluated against D. suzukii with most of them failing to develop from this host due to its strong host immune defense (Wang et al. 2020b). In the meantime, both G. brasiliensis and L. japonica have been unexpectedly detected in British Columbia, Canada and the state of Washington outside their presumed native range of Asia (Abram et al. 2020).

Of the known pupal parasitoids of drosophilids, two have been found to attack and develop successfully from D. suzukii: Pachycrepoideus vindemiae (Rondani) (Hymenoptera: Pteromalidae) and Trichopria drosophilae Perkins (Hymenoptera: Diapriidae) in Spain (Gabarra et al. 2015), Italy (Miller et al. 2015), Mexico (Garcia-Cancino et al. 2020), California (Wang et al. 2016), and Oregon (Miller et al. 2015). Both species are cosmopolitan and readily parasitize D. suzukii pupae inside fruit as well as in soil (Wang et al. 2016).

In comparison, information is currently lacking regarding the composition and distribution of resident parasitoid species of Drosophilidae in Michigan. This knowledge is important for the implementation of biological control against D. suzukii, especially prior to classical biological control agent releases. Moreover, this information will also aid in determining any possible non-target effects of parasitoids new to this region, with potential spillover effects to other Drosophilidae as well as potential interactions among resident and future introduced parasitoids (Hougardy et al. 2020). Thus, the objective of our survey was to determine the presence and biological control status of resident parasitoid populations in Michigan cherry orchards and natural habitats using sentinel banana traps infested with larvae or pupae of D. suzukii as hosts, in support of the development of biological control programs that may include future augmentative releases of parasitoids to suppress populations of D. suzukii.

In total, 1 adult parasitoid was captured, at least 1876 parasitoids were reared out from the sentinel cups. Three species of parasitoids were either found in traps or emerged from cups baited with sliced banana infested with drosophila larvae or pupae: Pachycrepoideus vindemiae Rondani (Hymenoptera: Pteromalidae), Leptopilina boulardi Barbotin, Carton & Keiner-Pillault, and Leptopilina heterotoma (Thomoson) (Hymenoptera: Figitidae). Large numbers of P. vindemiae and L. boulardi emerged from sentinel cups within 3–4 weeks after initial field collection. Pachycrepoideus vindemiae was present in all trapping sites, but L. boulardi was only found in northwest Michigan. A single specimen of L. heterotoma was found in a sentinel cup immediately following field collection in a commercial cherry orchard in west Michigan.

The first emergence of P. vindemiae was from sentinel traps deployed at central Michigan sites during the week of 23 July. This species was abundant both in west and central Michigan throughout the sampling period (Fig. 1) and present in all 26 sentinel traps including those deployed in the northwest region at least once during the survey period. In total, 1319 P. vindemiae emerged from sentinel traps at sites in west Michigan compared to 557 P. vindemiae in central Michigan. Sentinel traps placed in orchards had significantly higher P. vindemiae emergence than those in the woodlots (F_1,15 = 5.14, P = 0.04) (Fig. 2A). Woodlots adjacent to orchards had significantly more P. vindemiae emerged than woodlots without cherry orchards nearby (F_1,10 = 7.83, P = 0.02) (Fig. 2B).

Figure 1. 

Total P. vindemiae emergence from weekly D. suzukii pupal sentinel traps in west Michigan (n = 6) and central Michigan (n = 11).

Figure 2. 

Mean total numbers of P. vindemiae (+SEM) emerged during a 14-week sampling period between sentinel traps placed in orchards vs. in woodlots regardless of orchards nearby (A), and between sentinel traps placed in woodlots adjacent to orchards and in those without orchards nearby (B). Asterisk indicates a significant difference between trap locations (P < 0.05).

Pachycrepoideus vindemiae successfully reproduced using D. suzukii pupae as its host under laboratory conditions. Hundreds of L. boulardi emerged from sentinel cups deployed in the northwest region, but none of them were able to reproduce on D. suzukii larvae.

This survey presents the first baseline data on the current field presence and seasonal occurrence of resident parasitoids of Drosophilid flies in Michigan. As expected, P. vindemiae was abundant and prevalent in Michigan since it attacks other pupae of many Dipteran fly families including Drosophilidae (Wang et al. 2004; Rossi Stacconi et al. 2013; Miller et al. 2015). Under controlled and optimal laboratory conditions, females of this species are capable of parasitizing nearly 600 D. suzukii pupae during their lifetime (Bezerra Da Silva et al. 2019). However, a field survey revealed low levels of parasitism of D. suzukii pupae in both North America and Europe (Lee et al. 2019; Wang et al. 2021), likely due in part to its relatively wide host range (Wang et al. 2021).

Larval parasitoids such as L. boulardi, L. heterotoma, and Asobara tabida (Nees) are important natural enemies of many endemic Drosophilidae species, but rarely successfully parasitize D. suzukii larvae (Girod et al. 2018). Although, hundreds of L. boulardi emerged from sentinel traps originally baited with D. suzukii larvae in northwest Michigan, none of them successfully reproduced on D. suzukii in the laboratory due to a strong immune response by the host. This indicates that other drosophilid species re-colonized D. suzukii infested banana slices, attracting larval parasitoids such as L. boulardi and L. heterotoma for oviposition. Indeed, other Drosophilidae including D. melanogaster were observed emerging from some of the sentinel traps after being incubated in the laboratory.

One potential reason why D. suzukii is so destructive to cultivated fruit crops is the absence of a significant natural enemy in invaded regions. Recently, G. brasiliensis, a species-specific larval parasitoid imported from Asia (Daane et al. 2016; Giorgini et al. 2019) that attacks early instar D. suzukii larvae (Wang et al. 2018), has been approved for release in Michigan as a classical biological control agent. While it is expected to take time for new natural enemies such as G. brasiliensis to suppress D. suzukii populations, resident pupal parasitoids such as P. vindemiae and T. drosophilae could play an important role through augmentative releases in combination with releases of new natural enemies. Interestingly, P. vindemiae has recently been found to parasitize and successfully develop on all preimaginal stages of G. brasiliensis (Hougardy et al. 2022), which could also potentially affect the establishment and success of G. brasiliensis.

Importantly, P. vindemiae was found most abundantly within cherry orchards after harvest, suggesting that they can navigate this agroecosystem despite presumable remnants of chemical applications commonly present in these systems. However, this may also imply that they are present during the growing season when regular insecticide applications are applied, suggesting possible disruption of this biological control from chemical exposure. More information is needed to elucidate the effects of pesticide, both in-season and post-harvest, on the success of current and future biological controls for D. suzukii. Additionally, P. vindemiae was more commonly associated with woodlots adjacent to cultivated cherry, likely because D. suzukii and other Drosophila populations are higher in areas with greater access to host fruit. This study serves as baseline information for the resident parasitoid community of Drosophilidae in the tart cherry agroecosystem and provides guidance on landscape factors that influence establishment of future augmentative and classical biological control releases.

We thank Brandon Byiringiro, Eric Zhang, Mohammad Turani, and Claire Komarzec for their assistance in rearing insect colonies and the field surveys. We also thank Karen Powers for conducting the field survey in northwest Michigan and growers for access to their farms throughout Michigan. This research was supported in part by the Michigan Cherry Committee. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the USDA. USDA is an equal opportunity provider and employer.