Brian N. Hogg

Invasive exotic arthropods and weeds pose a growing threat to biodiversity, food security, and the functioning of whole ecosystems, resulting in significant socioeconomic and ecological impacts. Classical biological control—the importation of specialist natural enemies from the native range—can lead to long-term, sustainable pest suppression, but it is typically implemented reactively after the invasive species is established and is causing significant negative impacts. Proactive biological control offers an anticipatory approach, developing biological control agents before or shortly after establishment and enabling rapid response to new incursions. This review examines current applications, opportunities, and challenges of proactive strategies and proposes steps to advance proactive management of invasive arthropod pests and weeds.

The invasive pest spotted wing drosophila, Drosophila suzukii (Matsumura), attacks many wild and ornamental hosts and may persist in semi-natural habitats when fruit is unavailable in the crop. Semi-natural habitat or non-crop habitat (NCH) may also provide shelter for D. suzukii or refuge from insecticide applications. We examined population dynamics of D. suzukii in berry fields and adjacent NCH over 3 growing seasons and sampled at different distances from NCH to determine whether NCH is a source for D. suzukii and its parasitoids in adjacent crop fields. Numbers of D. suzukii adults were higher in NCH on most sample dates and increased in berry fields with proximity to NCH in spring and fall, indicating that NCH was a refuge and source for D. suzukii. Proportions of female D. suzukii were higher in berry fields in spring and fall and increased with distance from NCH along transects, suggesting that females dispersed more widely in berry fields than males. NCH did not appear to be a significant source of D. suzukii in summer, when D. suzukii numbers tended to be similar between habitats and did not change along transects within berry fields. Parasitism of sentinel D. suzukii pupae by the dominant naturally occurring parasitoid Trichopria drosophilae (Perkins) did not differ between NCH and berry fields, indicating that T. drosophilae dispersed easily between habitats.

Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) has become a damaging economic pest of small fruits in the invaded range in the Americas, Europe, and North Africa. This study surveyed naturally occurring parasitoids of D. suzukii and other frugivorous Drosophilidae in California’s coastal and interior fruit production regions. Surveys were conducted from 2012 to 2018 through collections of infested fruits and the use of sentinel fruit or host traps. Two pupal parasitoids, Pachycrepoideus vindemiae (Rondani) (Hymenoptera: Pteromalidae) and Trichopria drosophilae (Perkins) (Hymenoptera: Diapriidae) were collected from D. suzukii and other drosophilids; the former species dominated in the interior while the latter species dominated in the coastal region. Two larval parasitoids, Leptopilina boulardi Barbotin et al. and L. heterotoma (Thomson) (Hymenoptera: Figitidae) were collected from drosophilid species other than D. suzukii, and were the dominant parasitoids in the interior and coastal regions, respectively. These four common parasitoids were most active during the spring and fall. The levels of parasitism on D. suzukii were < 10% from field-collected fruits but were as high as 74% in sentinel traps. Pupal parasitoids attacked D. suzukii at a higher rate than D. melanogaster in sentinel traps baited with both fly species. These results are discussed in conjunction with ongoing efforts to introduce larval parasitoids from the fly’s native range.

Programs to mass rear and release Ganaspis kimorum Buffington (Hymenoptera: Figitidae) are ongoing in many countries to manage its host Drosophila suzukii (Matsumura) (Diptera: Drosophilidae). To optimize parasitoid production and synchronize field releases with pest outbreaks, we investigated a cold storage protocol by exposing different immature G. kimorum stages to 2 storage temperatures (10 or 15°C) for 2, 4, 6, or 8 wk. We further studied those temperature/exposure time combinations that allowed survival but prevented parasitoid emergence before the end of each cold exposure, or the cold storage suitability (CSS). The impact of cold storage on G. kimorum emergence time, total development time, and emergence rate was then evaluated for temperature/exposure time combinations with CSS > 60%. We also assessed fitness costs in terms of longevity and parasitism rates of emerging parasitoids. Results showed that only G. kimorum larvae and pupae were suitable for cold storage under this methodology. Cold exposure significantly delayed the emergence time and total development time of larvae and pupae, whereas the emergence rate was significantly reduced only for larvae at 10°C for 6 wk. The longevity of emerging male and female parasitoids was significantly reduced when stored cold as larvae, while no effects were reported for the parasitism rate by emerged females. These findings provide new insights into G. kimorum cold sensitivity and offer valuable options to better schedule mass rearing and wasp releases for biological control of D. suzukii.

Bagrada bug, Bagrada hilaris (Burmeister) (Hemiptera: Pentatomidae), is an invasive pest of cole crops in the United States. Because it also feeds on widespread weeds and persists in natural habitats surrounding crop fields, conventional control strategies are often ineffective at providing long-term control. One egg parasitoid, Gryon aetherium Talamas (Hymenoptera: Scelionidae), is a promising biological control candidate because of its ability to parasitise B. hilaris buried eggs. Recently, adventive populations of G. aetherium were recovered from sentinel eggs in California along with a native egg parasitoid, Ooencyrtus californicus Girault (Hymenoptera: Encyrtidae). A better understanding of these parasitoid species’ spatial preference for foraging and their possible competitive interactions will help evaluate their host suppression potential. We compared the foraging abilities of these two parasitoid species for eggs deposited below and above ground. We also investigated the effect of interspecific competition on host suppression and the ability of O. californicus to parasitise eggs previously parasitised by G. aetherium. G. aetherium parasitised naturally and manually buried eggs, whereas O. californicus did not. In another experiment, O. californicus parasitised eggs glued to cards, but not in the presence of sand. Results suggest that G. aetherium may be negatively affected by the presence of O. californicus, and there was a slight but significant reduction in total host mortality when the parasitoids were present together. However, the inability of O. californicus to forage in soil likely limits negative interactions between these two species, and the two parasitoids may ultimately complement each other.

Spotted wing drosophila, Drosophila suzukii , has become a major pest of soft‐skinned fruit crops in the Americas, Europe and North Africa. In many regions, D. suzukii management is complicated by the fly's ability to persist on non‐crop hosts and then invade or reinvade crop fields from surrounding natural habitats. In California, non‐crop habitats adjacent to commercial cane berry fields often contain wild blackberry ( Rubus spp.), a potential overwintering host for D. suzukii . We sampled D. suzukii and its naturally occurring parasitoids (the pupal parasitoids Trichopria drosophilae and Pachycrepoideus vindemmiae ) in commercial berry fields and adjacent non‐crop habitat throughout the year, to determine whether non‐crop habitat is a seasonal or year‐round refuge for D. suzukii , and whether numbers of D. suzukii and its parasitoids in berry fields are dependent on the composition of the surrounding landscape. Numbers of D. suzukii adults were consistently higher in non‐crop habitat, and proportions of female D. suzukii were highest in berry fields, indicating that females dispersed more widely than males. The effect of habitat diversity on numbers of D. suzukii adults was positive in fall and negative in early spring, possibly reflecting differing habitat requirements of D. suzukii over time. Parasitoid numbers were also higher in non‐crop habitat and were positively affected by proportions of non‐crop habitat and cropland in summer. Results indicate that non‐crop habitats were a year‐round refuge for both D. suzukii adults and its parasitoids, and that landscape effects on D. suzukii abundance in crop fields can change over the seasons.

Sentinel eggs used to monitor field parasitism of stink bug pests (Hemiptera: Pentatomidae) can only be deployed for a few days to avoid releasing the pest in the monitored area. Using sterile eggs removes the risk of accidental pest introduction and extends deployment time. Freezing the eggs before deployment is one common method of sterilizing sentinel eggs. However, some egg parasitoid species have low or no parasitism on frozen eggs. In this study, X-ray irradiation was used to sterilize Bagrada hilaris sentinel eggs intended for monitoring parasitism by Gryon aetherium (Hymenoptera: Scelionidae), the most promising biological control candidate. In this case, freezing sentinel eggs is not recommended because G. aetherium has low levels of parasitism on frozen eggs. Doses as low as 10 Gy induced 100% sterility. Irradiated eggs successfully sustained the development of G. aetherium and Ooencyrtus californicus (Hymenoptera: Encyrtidae), another egg parasitoid attacking B. hilaris, and parasitism levels were comparable to that of fresh eggs up to seven days old. In addition, G. aetherium showed no preference for fresh non-irradiated eggs over seven-day-old irradiated eggs. Our results indicate that X-ray irradiation is a suitable alternative to produce safe and reliable sentinel eggs to monitor the egg parasitism of B. hilaris and possibly other species.

Sentinel eggs used to monitor field parasitism of stink bug pests (Hemiptera: Pentatomidae) can only be deployed for a few days to avoid releasing the pest in the monitored area. Using sterile eggs removes the risk of accidental pest introduction and extends deployment time. Freezing the eggs before deployment is one common method for sterilizing sentinel eggs. However, some egg parasitoid species have lower to no parasitism on frozen eggs. In this study, x-ray irradiation was used to sterilize Bagrada hilaris sentinel eggs intended for monitoring parasitism by Gryon aetherium (Hymenoptera: Scelionidae), the most promising biological control candidate. In this case, freezing sentinel eggs is not recommended because G. aetherium has low levels of parasitism on frozen eggs. Doses as low as 10 Gy induced 100% sterility. Irradiated eggs successfully sustained the development of G. aetherium and Ooencyrtus californicus (Hymenoptera: Encyrtidae), another egg parasitoid attacking B. hilaris, and parasitism levels were comparable to fresh eggs up to seven days. In addition, G. aetherium showed no preference for fresh non-irradiated over seven-day-old irradiated eggs. Our results indicate that x-ray irradiation is a suitable alternative to produce safe and reliable sentinel eggs to monitor egg parasitism of B. hilaris and possibly other species.

Bagrada bug, Bagrada hilaris (Burmeister) (Hemiptera: Pentatomidae), is an invasive pest of cruciferous crops. The parasitoid Gryon aetherium Talamas (Hymenoptera: Scelionidae) is a promising biological control agent for B. hilaris because it can forage in the soil where B. hilaris deposits most of its eggs. In this study, we assessed parasitism by G. aetherium on B. hilaris eggs in situ in northcentral California, including the Salinas Valley where most cruciferous crops in the United States are grown. Parasitism was documented by leaving soil-filled trays under infested plants for 7–14 days, then removing eggs and holding them for emergence of parasitoids. Gryon aetherium accounted for over 99% of emerged parasitoids, and occurred at 11 of the 12 sampled sites. Of the 17,729 and 31,759 B. hilaris eggs collected in 2021 and 2022, 1,518 (8.84%) and 2,654 (8.36%) were parasitized by G. aetherium, respectively. Parasitism rates were generally higher inland and ranged from 3.64% to 44.93% in 2021 and from 1.01% to 23.04% in 2022, and never exceeded 15% on any sample dates at several coastal sites in the Salinas Valley. Discovery efficiency (a measure of the ability of parasitoids to locate egg patches) reached 80% or higher at all but 1 site, but exploitation efficiency (a measure of the ability of parasitoids to exploit the egg patch after it has been discovered) was generally G. aetherium can locate egg patches efficiently but is less efficient at finding eggs within patches.