Floral resources enhance fitness of the parasitoid Hadronotus pennsylvanicus (Hymenoptera: Scelionidae) but not biological control of its host Leptoglossus zonatus (Heteroptera: Coreidae).

The diet of adult parasitoid wasps is vital for their survival and reproduction. However, the availability of food resources, such as plant nectar, can vary widely in cropping systems, potentially affecting parasitoid fitness and thereby biological control of pests. The egg parasitoid Hadronotus pennsylvanicus (Ashmead) (Hymenoptera: Scelionidae) is a potential biological control agent of the pistachio pest Leptoglossus zonatus (Dallas) (Heteroptera: Coreidae). While H. pennsylvanicus is known to attack L. zonatus eggs in California, USA, parasitism rates in orchards are highly variable. Floral resource provisioning has the potential to enhance parasitoid longevity and thus improve parasitism rates, leading to reduced pest densities. Here, a combination of field and laboratory studies was used to assess the influence of flowering groundcovers on the reproductive fitness of H. pennsylvanicus and the abundance of L. zonatus. Evaluated groundcovers included oat (Avena sativa L.), cowpea (Vigna unguiculata L.), white mustard (Sinapis alba L.), and buckwheat (Fagopyrum esculentum Moench). Under laboratory conditions, buckwheat and mustard provided the greatest benefit to female H. pennsylvanicus longevity. However, females provided a buckwheat diet produced the greatest number of offspring over the course of their lifetime. In field trials, flowering groundcovers did not influence the abundance of H. pennsylvanicus nor parasitism rates on L. zonatus. While the availability of floral resources can improve the reproductive fitness of H. pennsylvanicus, the use of groundcovers in pistachio did not enhance biological control of L. zonatus.

Alterations in Ferrisia gilli (Hemiptera: Pseudococcidae) phenology in California pistachios and potential impacts on controls.

The mealybug, Ferrisia gilli Gullan, attacks important crops such as almonds, grapes, and pistachios in California. In pistachios, F. gilli has 3 generations per year, and a single insecticide application timed to the presence of first instars of the first or second generation provided sufficient control. This strategy has, recently, become less effective, and here we tested the possible explanation that F. gilli life stages are smeared, with different life stages present concurrently, reducing the efficacy of a single pesticide application. We monitored F. gilli populations and their natural enemies in central California pistachio orchards from 2021 through 2022. We found the first generation of F. gilli was synchronous, but occurred 3 wk earlier than previously reported. Subsequent generations were smeared. Increased yearly temperatures are a likely explanation for the changes observed in phenology. Almost all natural enemies found were lacewings (n > 10,000). Parasitoids were recovered from pistachios in 2021 (n = 4) and 2022 (n = 164), most were hyperparasitoids. Based on these studies, recommendations are made to monitor F. gilli in early May rather than late May to better target insecticide applications for the first instars.

Reproductive biology of overwintering leaffooted bug Leptoglossus zonatus (Hemiptera: Coreidae) in California.

Leptoglossus zonatus (Dallas) (Hemiptera: Coreidae) is a polyphagous insect pest attacking a wide variety of crops. In California's Central Valley, it is now the dominant leaffooted bug on almonds, pistachios, and pomegranates. Leptoglossus zonatus pest status depends largely on overwintering adult survival and reproductive potential, which determines its population size in spring and early summer when nut crops are particularly susceptible to bug damage. Here, we investigated the overwintering reproductive biology of L. zonatus in laboratory and field experiments to gain information about its ovary development, time of mating, and the impact of low temperatures on egg hatch. With dissections of laboratory-reared L. zonatus, we established a baseline for ovarian development and determined that the size of the spermathecal reservoir is larger in mated than in unmated females. Dissections and behavioral experiments of field-collected material provided evidence of mating events before dispersal from overwintering sites. Laboratory trials showed that temperature significantly impacted L. zonatus egg hatch. Leptoglossus zonatus reproductive biology presented provides valuable information on its population dynamics and dispersal from overwintering sites, and will contribute to the development of monitoring and management tools.

Evaluating invasion risk and population dynamics of the brown marmorated stink bug across the contiguous United States.

BACKGROUND: Invasive species threaten the productivity and stability of natural and managed ecosystems. Predicting the spread of invaders, which can aid in early mitigation efforts, is a major challenge, especially in the face of climate change. While ecological niche models are effective tools to assess habitat suitability for invaders, such models have rarely been created for invasive pest species with rapidly expanding ranges. Here, we leveraged a national monitoring effort from 543 sites over 3 years to assess factors mediating the occurrence and abundance of brown marmorated stink bug (BMSB, Halyomorpha halys), an invasive insect pest that has readily established throughout much of the United States. RESULTS: We used maximum entropy models to estimate the suitable habitat of BMSB under several climate scenarios, and generalized boosted models to assess environmental factors that regulated BMSB abundance. Our models captured BMSB distribution and abundance with high accuracy, and predicted a 70% increase in suitable habitat under future climate scenarios. However, environmental factors that mediated the geographical distribution of BMSB were different from those driving abundance. While BMSB occurrence was most affected by winter precipitation and proximity to populated areas, BMSB abundance was influenced most strongly by evapotranspiration and solar photoperiod. CONCLUSION: Our results suggest that linking models of establishment (occurrence) and population dynamics (abundance) offers a more effective way to forecast the spread and impact of BMSB and other invasive species than simply occurrence-based models, allowing for targeted mitigation efforts. Implications of distribution shifts under climate change are discussed. © 2022 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Methods for Rearing the Parasitoid Ganaspis brasiliensis, a Promising Biological Control Agent for the Invasive Drosophila suzukii.

Native to East Asia, the spotted-wing drosophila, Drosophila suzukii (Matsumura) (Diptera: Drosophilidae), has established widely in the Americas, Europe, and parts of Africa over the last decade, becoming a devastating pest of various soft-skinned fruits in its invaded regions. Biological control, especially by means of self-perpetuating and specialized parasitoids, is expected to be a viable option for sustainable area-wide management of this highly mobile and polyphagous pest. Ganaspis brasiliensis Ihering (Hymenoptera: Figitidae) is a larval parasitoid that is widely distributed in East Asia, and has been found to be one of the most effective parasitoids of D. suzukii. Following rigorous pre-introduction evaluations of its efficacy and potential non-target risks, one of the more host-specific genetic groups of this species (G1 G. brasiliensis) has been approved recently for introduction and field release in the United States and Italy. Another genetic group (G3 G. brasiliensis), which was also commonly found to attack D. suzukii in East Asia, may be considered for introduction in the near future. There is currently enormous interest in rearing G. brasiliensis for research or in mass-production for field release against D. suzukii. This protocol and associated video article describe effective rearing methods for this parasitoid, both on a small scale for research and a large scale for mass-production and field release. These methods may benefit further long-term research and use of this Asian-native parasitoid as a promising biological control agent for this global invasive pest.

Comparative Life History Parameters of Three Stink Bug Pest Species.

California pistachios are threatened by several stink bug species (Hemiptera: Pentatomidae), including the native Thyanta pallidovirens (Stål) and Chlorochroa uhleri (Stål), as well as the invasive Nezara viridula (L.). In pistachio, control tactics often target specific life stages, which makes knowledge about life histories fundamental to successful IPM programs. For that purpose, life history parameters of these stink bug species were assessed. Nymphal development and survivorship at seven constant temperatures, upper and lower development thresholds, thermal constants, adult longevity and fecundity, and life table parameters were evaluated. No species completed development at 15°C or 35°C. For N. viridula, egg to adult development was fastest at 30°C, whereas for T. pallidovirens there was no significant difference between 27.5 and 30°C and C. uhleri development was similar between 25 and 30°C. Egg to adult survival was highest at 22.5°C and 27.5°C. The thermal requirements as degree-days (DD) to complete immature development were estimated to be 714.3, 370.4, and 434.8 for C. uhleri, T. pallidovirens, and N. viridula, respectively. For C. uhleri, life table calculations produced a value of 56.7 d for mean generation time (To), 24.89 for net reproductive rate (Ro) and 0.057 for the intrinsic rate of increase (r). Thyanta pallidovirens had a To of 39.9 d, a Ro of 81.10 and a r of 0.11. The results are discussed with respect to the improvement of IPM in California pistachios, and the information presented may contribute to the control of these pest species in other ecosystems.

Field Survival of the Brown Marmorated Stink Bug Halyomorpha halys (Hemiptera: Pentatomidae) on California Tree Crops.

Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) is a polyphagous insect pest that has invaded much of the United States, including California. Despite model predictions that regions in California like the agriculturally important Central Valley are suitable, H. halys populations and the occurring crop damage are distinctly lower than in regions of the East Coast. To evaluate if this is due to low nymphal survival in the high temperature and intensive monoculture environment, H. halys nymphs were caged on four common Central Valley tree crops: almond, pistachio, peach, and grape, and compared to the well-established almond and pistachio pest Leptoglossus zonatus (Dallas) (Hemiptera: Coreidae). Nymphal development showed that peach, almond, and pistachio can sustain H. halys as single host plants until adult eclosion, whereas grapes cannot. The addition of fruiting structures of almond, pistachio, and grape to H. halys caged on peach trees (= mixed diet) did not increase nymphal survival but did increase adult female size. Leptoglossus zonatus survival was higher than H. halys on pistachio, but not on the other crops. Overall, H. halys nymphal mortality in the field was high, with 92% in the mixed diet compared to 73% in the mixed diet control in the laboratory, indicating abiotic population pressures. Our results confirm peach as a good H. halys host plant and suggest that almond has a similar suitability, and while pistachios can support H. halys nymphal development, they seem less likely to facilitate population growth.

Comparing the Feeding Damage of the Invasive Brown Marmorated Stink Bug to a Native Stink Bug and Leaffooted Bug on California Pistachios.

California currently produces about a quarter of the world's pistachios. Pistachio nuts are susceptible to feeding by stink bugs and leaffooted bugs; therefore, the invasive presence of the highly polyphagous brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), is a concern to California pistachio growers. We aimed to assess the potential of H. halys to cause yield loss and nut damage to pistachios, which had not yet been assessed in the field. Over two years, terminal branch ends with pistachio clusters were enclosed in organdy cages from spring to fall and exposed to either H. halys, the native stink bug Chinavia hilaris Say (Hemiptera: Pentatomidae), or leaffooted bug Leptoglossus zonatus (Dallas) (Hemiptera: Coreidae), for 4-7-day feeding periods at different times of the season. We found that H. halys adults cause more epicarp lesions (external damage) when recorded at harvest time than the native species. They did not, however, cause more kernel necrosis (internal damage) than the two native species tested, which is a more relevant damage criterion for commercial production. There were no differences among insect species for any other recorded damage criteria. We conclude that H. halys could cause similar damage as the native species but note that H. halys population densities in California are still low and future damage levels will be dependent on this pest's population density.

Next-generation biological control: the need for integrating genetics and genomics.

Biological control is widely successful at controlling pests, but effective biocontrol agents are now more difficult to import from countries of origin due to more restrictive international trade laws (the Nagoya Protocol). Coupled with increasing demand, the efficacy of existing and new biocontrol agents needs to be improved with genetic and genomic approaches. Although they have been underutilised in the past, application of genetic and genomic techniques is becoming more feasible from both technological and economic perspectives. We review current methods and provide a framework for using them. First, it is necessary to identify which biocontrol trait to select and in what direction. Next, the genes or markers linked to these traits need be determined, including how to implement this information into a selective breeding program. Choosing a trait can be assisted by modelling to account for the proper agro-ecological context, and by knowing which traits have sufficiently high heritability values. We provide guidelines for designing genomic strategies in biocontrol programs, which depend on the organism, budget, and desired objective. Genomic approaches start with genome sequencing and assembly. We provide a guide for deciding the most successful sequencing strategy for biocontrol agents. Gene discovery involves quantitative trait loci analyses, transcriptomic and proteomic studies, and gene editing. Improving biocontrol practices includes marker-assisted selection, genomic selection and microbiome manipulation of biocontrol agents, and monitoring for genetic variation during rearing and post-release. We conclude by identifying the most promising applications of genetic and genomic methods to improve biological control efficacy.

Can Anastatus bifasciatus Be Used for Augmentative Biological Control of the Brown Marmorated Stink Bug in Fruit Orchards?

The generalist egg parasitoid Anastatus bifasciatus (Geoffroy) (Hymenoptera: Eupelmidae) is the most prevalent egg parasitoid of the invasive Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) in Europe. To assess its efficacy against the pest H. halys and to validate the potential risks for non-target species in a realistic field setting, inundative releases were conducted over three consecutive years in four fruit orchards in Switzerland and Italy. In total, more than 4300 A. bifasciatus females were released, which was equivalent to 11,000 to 26,000 females per hectare, depending on distances between trees in each orchard. Parasitism of freeze-killed sentinel H. halys eggs achieved with the current release strategy was on average 6% (range: 2%-16%) and considered not high enough to effectively suppress the pest. However, the overall impact of A. bifasciatus on the mortality of H. halys eggs was likely underestimated. If pre-imaginal parasitoid mortality (3.3%) and host feeding (6%) are added to the observed parasitism (6%), the actual induced mortality of H. halys eggs may reach more than 15%. Parasitism of lepidopteran non-target species reached an average of 8% and thus, some degree of non-target parasitism after mass releases may be expected. To quantify the impact of the parasitoids in the orchards more precisely, naturally laid egg masses should be used in future trials to include host-finding cues of the host and host plants, and larger scale releases with potentially higher densities of parasitoids should be considered.

Using the egg parasitoid Anastatus bifasciatus against the invasive brown marmorated stink bug in Europe: can non-target effects be ruled out?

The brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), has been causing massive damage to various fruit and vegetable crops after its arrival in the USA, and more recently in Europe. To provide an alternative control measure to pesticides, the native egg parasitoid Anastatus bifasciatus (Geoffroy) (Hymenoptera: Eupelmidae) was considered as a candidate biological control agent for inundative releases in Europe. In the risk assessment study presented here, all nine heteropteran and 14 out of 19 tested lepidopteran non-target species produced viable A. bifasciatus offspring. The proportion of A. bifasciatus females producing offspring did not differ between non-target and target for 19 out of the 28 non-target species. Larger host eggs corresponded to increased female-biased sex ratio of the offspring as well as an increase in size, particularly for females, with hind tibia lengths varying from 645.5 ± 46 to 1084 ± 28.5 µm. Larger females were also found to have higher offspring production and increased life expectancy. The results of this study confirmed the polyphagous nature of A. bifasciatus and suggest that a number of non-target species, including Lepidoptera of conservation interest, may be attacked in the field. Thus, non-target effects cannot entirely be ruled out, but more information is needed from semi-field and field studies to fully assess potential environmental risks due to inundative releases of this native parasitoid.