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.

Diet quality influences nutrient retention and reproductive fitness of the biocontrol agent Hadronotus pennsylvanicus (Hymenoptera: Scelionidae).

Diet can have a direct influence on the reproductive success of parasitoid wasps. For synovigenic parasitoids, the nutrients obtained from floral resources, such as nectar and pollen, play a vital role in fueling bodily functions and physiological energy expenditure incurred from reproduction. Insufficient access to nutrient-rich diets can lead to lower rates of reproductive fitness, therefore reducing the efficacy of biocontrol. Here, a study was conducted to evaluate the influence of diet quality on nutrient retention and reproductive fitness of the egg parasitoid Hadronotus pennsylvanicus (Hymenoptera: Scelionidae), a prospective biocontrol agent for the leaffooted bug Leptoglossus zonatus (Heteroptera: Coreidae), a primary pest of almonds and pistachios. Newly emerged parasitoid females were provided host eggs every other day accompanied by diets of varying sucrose concentrations (source of carbohydrates) and pollen (source of lipid and proteins). The sucrose concentration in the diet, regardless of pollen content, significantly increased the survival and lifetime fecundity of female H. pennsylvanicus. While wasps fed high sucrose diets depleted bodily sugars, glycogen, and lipids at a slower rate than wasps fed low sucrose diets, there was no effect on bodily protein levels. Given these findings, further research is now needed to identify floral resources that are compatible, attractive, and nutritionally-sufficient for optimal H. pennsylvanicus reproductive fitness, which could lead to enhanced parasitism of L. zonatus in crop systems.

Diel Periodicity in Males of the Navel Orangeworm (Lepidoptera: Pyralidae) as Revealed by Automated Camera Traps.

Navel orangeworm, Amyelois transitella (Walker), is a key pest of walnuts, pistachio, and almonds in California. Pheromone mating disruption using timed aerosol dispensers is an increasingly common management technique. Dispenser efficiency may be increased by timing releases with the active mating period of navel orangeworm. Past work found that the peak time of sexual activity for navel orangeworm females is 2 h before sunrise when temperatures are above 18°C. Inference of male responsiveness from data collected in that study was limited by the necessity of using laboratory-reared females as a source of sex pheromone emission to attract males and the inherent limitations of human observers for nocturnal events. Here we used camera traps baited with artificial pheromone to observe male navel orangeworm mating response in the field over two field seasons. Male response to synthetic pheromone exhibited diel patterns broadly similar to females, i.e., they were active for a brief period of 2-3 h before dawn under summer conditions and began responding to pheromone earlier and over a longer period of time during spring and fall. But contrary to the previous findings with females, some males were captured at all hours of the day and night, and there was no evidence of short-term change of pheromone responsiveness in response to temperature. Environmental effects on the response of navel orangeworm males to an artificial pheromone source differ in important ways from the environmental effects on female release of sex pheromone.

Identification and Synthesis of Leptotriene, a Unique Sesquiterpene Hydrocarbon from Males of the Leaffooted Bugs Leptoglossus zonatus and L. occidentalis.

The leaffooted bugs Leptoglossus zonatus and L. occidentalis (Hemiptera: Coreidae) cause substantial damage in tree nut crops in North America and pine seed orchards in North America and Europe, respectively. Sexually mature males of both species produce a number of aldehydes, esters, and sesquiterpenes, which are hypothesized to constitute an aggregation pheromone attractive to both sexes. Among the volatiles produced by males of both species, we identified a unique sesquiterpene hydrocarbon, given the common name "leptotriene" (5), which elicited strong responses from antennae of both sexes in electroantennogram assays. Here, we report its structure and its synthesis from (-)-(E)-ß-caryophyllene (1).

Winter Cover Crops Reduce Spring Emergence and Egg Deposition of Overwintering Navel Orangeworm (Lepidoptera: Pyralidae) in Almonds.

Habitat diversification has been shown to positively influence a variety of ecosystem services to agriculture, including biological control of arthropod pests. The impact of increased biodiversity tends to be species specific though, and practices therefore need to be developed on a case-by-case basis for each cropping system. In perennial systems, numerous studies have demonstrated that cover crops can have positive impacts on soil quality and other ecosystem services, such as pollination and pest management. However, few studies have focused on the use of cover crops to enhance pest control in almond orchards, especially winter cover crops. The primary pest of almonds in North America is navel orangeworm, Amyelois transitella Walker, which overwinter as larva or pupa on remnant nuts, many of which remain on the orchard soil surface. In the spring, first flight adults subsequently use these remnant nuts as reproductive substrate. An experiment was conducted to evaluate the influence of two distinct winter cover crop mixtures on overwintering mortality and spring egg deposition of A. transitella. Remnant nuts placed into cover crop plots produced fewer adult A. transitella in the spring, suggesting increased overwintering mortality. Additionally, spring egg deposition was reduced on remnant nuts in the cover crops, possibly due to the ground covers interfering with host location and access. In this way, winter cover crops appear to contribute to the reduction of A. transitella populations in the orchard by altering abiotic and physical conditions, although studies to document specific mechanisms are still needed.

Food deprivation alters reproductive performance of biocontrol agent Hadronotus pennsylvanicus.

Diet can influence parasitoid reproductive performance, and therefore, the efficacy of biocontrol programs. We evaluated the influence of food deprivation on the reproductive fitness and behavior of the egg parasitoid Hadronotus pennsylvanicus (Hymenoptera: Scelionidae), a prospective biocontrol agent for Leptoglossus zonatus (Heteroptera: Coreidae). Newly emerged female parasitoids were mated and provided host eggs every other day while being provisioned with various honey diet regimes or a consistent supply of water. When given frequent access to a honey diet, female parasitoids lived significantly longer and parasitized more host eggs compared to the water-fed controls. Once depleted of mature eggs, females with frequent access to honey also contributed to greater non-reproductive host mortality. Furthermore, behavioral assays demonstrated that water-fed females spent less time interacting with host eggs and tended to more frequently divert from oviposition behavior. While there was no difference in the average duration until first oviposition between individuals assigned to different diet treatments, increased frequency of honey feeding was associated with more frequent and longer duration of oviposition. The positive effect of honey feeding on the reproductive performance of biocontrol agent H. pennsylvanicus suggests that performance of this parasitoid under field conditions could be enhanced through the provision of similar carbohydrate resources, such as flowering summer cover crops.

Balancing Bees and Pest Management: Projected Costs of Proposed Bee-Protective Neonicotinoid Regulation in California.

Neonicotinoid insecticides are widely used in agriculture, including in many California specialty crops. With mounting evidence that these insecticides are harmful to bees, state and national governments have increasingly regulated their use. The European Union, Canada, and United States have imposed use restrictions on several neonicotinoids, such as on the timing of applications. In 2020, California proposed a draft regulation to mitigate harm to managed pollinators from four nitroguanidine-substituted neonicotinoids (NGNs): clothianidin, dinotefuran, imidacloprid, and thiamethoxam. We use data on California pesticide use from 2015 to 2017 to analyze the economic and pest management implications of the 2020 draft proposed regulation for seven crops: almond, cherry, citrus, cotton, grape, strawberry, and tomato. From 2015 to 2017, these crops accounted for approximately 85% of total hectares treated with NGNs and 87% of NGN use by kilograms of active ingredient applied in treatments that would have been affected by the proposed regulation. These insecticides often primarily target Hemipteran insect pests. In most cases there are alternatives; however, these are often more expensive per hectare and do not have the same residual effectiveness as the NGNs, which are systemic insecticides. Overall, we estimate that pest management costs for these crops would have increased an estimated $13.6 million in 2015, $12.8 million in 2016, and $11.1 million in 2017 if the 2020 draft proposed regulation had been in effect, representing a 61% to 72% increase in the cost of managing the target pests.

Evaluating Flight Performance of Mass-Reared and Irradiated Navel Orangeworm (Lepidoptera: Pyralidae) for Sterile Insect Technique.

Navel orangeworm (Pyralidae: Amyelois transitella) is a key pest of almonds and pistachios in California. Moths directly infest nuts which leads to reduced crop yield and quality, and infestation can predispose nuts to fungal pathogens that produce aflatoxins. While several integrated pest management strategies have been developed for A. transitella, studies have recently been initiated to explore the use of sterile insect technique (SIT) as an additional control tool. Mass-rearing, sterilization, and transportation methods originally developed for Pectinophora gossypiella (Lepidoptera: Gelechiidae) are currently being used for production of A. transitella in a mass-rearing facility, but the impacts of these processes on performance of A. transitella remain unclear. In this study, computerized flight mills were used to evaluate multiple flight parameters of mass-reared and irradiated A. transitella males and females relative to non-irradiated mass-reared moths and two strains of locally reared moths which were neither mass-reared nor irradiated. Mass-reared non-irradiated females performed similarly to both strains of locally reared females, flying a mean 9.4-11.8 km per night, whereas mass-reared and irradiated males and mass-reared non-irradiated males all flew shorter distances, in the range of 3.0-6.7 km per night. All of the mass-reared moths compared to locally reared moths had significantly more non-fliers that did not engage in more than two minutes of continuous flight. Findings from this study suggest that mass-rearing conditions reduce A. transitella flight capacity, while irradiation interacts with moths in a sex-specific manner.

Use of Ground Covers to Control Three-Cornered Alfalfa Hopper, Spissistilus festinus (Hemiptera: Membracidae), and Other Suspected Vectors of Grapevine Red Blotch Virus.

Grapevine red blotch virus (GRBV) is the causal agent of grapevine red blotch disease, which affects wine grapes and leads to reduced crop yield and quality. The pathogen-plant-vector relationship of GRBV is not well understood; however, some possible vectors have been identified: Caladonus coquilletti (Van Duzee; Hemiptera: Cicadellidae), Colladonus reductus (Van Duzee; Hemiptera: Cicadellidae), Erythroneura spp., Melanoliarus sp. (Hemiptera: Cixiidae), Osbornellus borealis DeLong. & Mohr (Hemiptera: Cicadellidae), Scaphytopius granticus (Ball; Hemiptera: Cicadellidae), Spissistilus festinus (Say). Of these species, S. festinus has been shown to transmit the virus to uninfected grapevines, making it of particular interest. Since the pathogen-plant-vector relationship of GRBV is not yet completely understood, pesticide use is not necessarily the best way to manage these possible vectors. Here we test if ground cover removal, by discing in spring, could reduce the activity of potential GRBV vectors. We show that S. festinus presence in the canopy was reduced in disc rows compared to just mowing the ground vegetation, whereas there were no differences in presence in the canopy between disc and mow rows of the other possible insect vectors. Erythroneura elegantula (Osborn; Hemiptera: Cicadellidae), a common pest of grapevines but not a candidate GRBV vector, was found to have higher densities in the canopy in disc rows compared to mow rows, an effect possibly mediated by changes in vine vigor associated with ground covers. We conclude that if S. festinus is a primary vector of GRBV, discing ground covers in early spring may be a viable way to reduce their presence in the vine canopy.

Evaluating Response of Mass-Reared and Irradiated Navel Orangeworm, Amyelois transitella (Lepidoptera: Pyralidae), to Crude Female Pheromone Extract.

The navel orangeworm, Amyleois transitella (Lepidoptera: Pyralidae), is a key pest of almonds and pistachios in California. Larvae directly feed on nuts, reducing quality and yield, and adults can introduce fungi that produce aflatoxins. The development of sterile insect technique (SIT) is currently being explored as a management tool for this pest. Large quantities of A. transitella are mass-reared, irradiated, and shipped to California from a USDA APHIS facility in Phoenix, AZ. Preliminary field releases of sterile A. transitella from this facility resulted in poor recovery of males in pheromone traps, raising concerns that mass-reared male A. transitella may not be responding to pheromone from virgin females. In this study, a wind tunnel was used to evaluate the response of both irradiated and non-irradiated mass-reared A. transitella males to crude pheromone extract from females, and their performance was compared to two strains of locally reared non-irradiated A. transitella. While initial responses associated with pheromone detection where similar between mass-reared and locally reared moths, a lower proportion of the mass-reared moths ultimately made contact with the pheromone source. Surprisingly, the addition of irradiation did not further decrease their performance. While mass-reared moths respond to pheromone, their ability to locate and make contact with the pheromone source appears to be impeded. The underlying mechanism remains unclear, but is likely related to damage incurred during the mass-rearing and shipping process.

Influence of Riparian Habitat and Ground Covers on Threecornered Alfalfa Hopper (Hemiptera: Membracidae) Populations in Vineyards.

Grapevine red blotch virus (GRBV) is the causal agent of grapevine red blotch disease, which affects wine grapes and leads to reduced crop yield and quality. While some virus spread can be attributed to the propagation of infected plant material, a greenhouse assay recently demonstrated that the threecornered alfalfa hopper (Membracidae: Spissistilus festinus Say) can transmit GRBV between grapevines. While S. festinus is not considered an economic pest of wine grapes, this species is present in California vineyards and their feeding can cause petiole girdling. Recent surveys have noted a correlation between S. festinus populations and GRBV-positive vines in vineyard areas adjacent to riparian habitat. Here, S. festinus populations were monitored over a 2-yr period at multiple vineyard sites adjacent to riparian habitats. At each site, insects were sampled from ground covers and the vine canopy at the vineyard edge and interior, and vines in both locations were evaluated for petiole girdling. Results indicate that there was no difference in abundance of S. festinus at the vineyard edge and interior. Populations in the vine canopy were highest in the late spring and early summer, and this was followed by the appearance of petiole girdling, indicating a key period of potential GRBV transmission. Furthermore, activity in the vine canopy appears to be amplified when the quality of ground covers is reduced as the season progresses. That said, overall populations of S. festinus were relatively low and additional work is needed to characterize the timing and efficiency of transmission under field conditions.

Optimizing Trap Characteristics to Monitor the Leaffooted Bug Leptoglossus zonatus (Heteroptera: Coreidae) in Orchards.

The leaffooted bug, Leptoglossus zonatus (Heteroptera: Coreidae), has become a key pest of almonds, pistachios, and pomegranates in California. Adults and nymphs directly feed on nuts and fruits, which reduces crop yield and quality and can facilitate pathogen infections. Current monitoring strategies require growers to actively sample the tree canopy, with no economic thresholds being developed for this pest. To improve monitoring of L. zonatus, a three-year study was conducted to identify an optimal trap. A hanging cross-vane panel trap was identified as the best trap type in Year 1, and subsequent work in Years 1-3 focused on refining its use by modifying surface texture and color. Results indicated that coating trap surfaces with the lubricant fluon improved trap catching ability, and adults were most frequently recovered in yellow traps. A hanging cross-vane panel trap with these features could serve as the basis for the development of a new monitoring system for this pest in orchards, which could be improved further if semiochemical lures will be developed.

Seasonal Dynamics of the Leaffooted Bug Leptoglossus zonatus and Its Implications for Control in Almonds and Pistachios.

Leptoglossus zonatus is a polyphagous pest found throughout much of the Western Hemisphere. In California, L. zonatus attacks almond, pistachio, pomegranate, and walnut crops, but the seasonal use of and economic damage to these crops varies. To better understand the seasonal changes of L. zonatus populations and to improve monitoring programs in California's San Joaquin Valley, we caged overwintering adult males and females and then followed the resulting population dynamics over a one-year period. There were three generations over the one-year period, although eggs, nymphs, and adults overlapped among successive generations. From an initial 75 overwintering adult females, there were 1214 egg strands, 16,692 nymphs, and 4900 adults recorded during the one-year period. Depending on the generation, the number of nymphs per egg strand ranged from 11.3 to 14.3; the sex ratio was close to 1:1 with the exception of one female-biased cage; and nymph mortality ranged from 22.0% to 39.5%. Adult females isolated from each generation produced 2.4-5.1 egg strands per female that totaled 41.7-61.7 eggs per female with a 67.1-86.8% successful hatch rate. We find that the adult is the overwintering stage, as more adults (without food provisions) survived the winter compared to medium-sized or large-sized nymphs provided with both food and water. The results are discussed with respect to the development of L. zonatus control and monitoring programs for California's multi-billion-dollar (US) nut crops.

Summer Flowering Cover Crops Support Wild Bees in Vineyards.

Agricultural expansion and intensification negatively affect pollinator populations and has led to reductions in pollination services across multiple cropping systems. As a result, growers and researchers have utilized the restoration of local and landscape habitat diversity to support pollinators, and wild bees in particular. Although a majority of studies to date have focussed on effects in pollinator-dependent crops such as almond, tomato, sunflower, and watermelon, supporting wild bees in self-pollinated crops, such as grapes, can contribute to broader conservation goals as well as provide other indirect benefits to growers. This study evaluates the influence of summer flowering cover crops and landscape diversity on the abundance and diversity of vineyard bee populations. We showed that diversity and abundance of wild bees were increased on the flowering cover crop, but were unaffected by changes in landscape diversity. These findings indicate that summer flowering cover crops can be used to support wild bees and this could be a useful strategy for grape growers interested in pollinator conservation as part of a broader farmscape sustainability agenda.

Review of Ecologically-Based Pest Management in California Vineyards.

Grape growers in California utilize a variety of biological, cultural, and chemical approaches for the management of insect and mite pests in vineyards. This combination of strategies falls within the integrated pest management (IPM) framework, which is considered to be the dominant pest management paradigm in vineyards. While the adoption of IPM has led to notable and significant reductions in the environmental impacts of grape production, some growers are becoming interested in the use of an explicitly non-pesticide approach to pest management that is broadly referred to as ecologically-based pest management (EBPM). Essentially a subset of IPM strategies, EBPM places strong emphasis on practices such as habitat management, natural enemy augmentation and conservation, and animal integration. Here, we summarize the range and known efficacy of EBPM practices utilized in California vineyards, followed by a discussion of research needs and future policy directions. EBPM should in no way be seen in opposition, or as an alternative to the IPM framework. Rather, the further development of more reliable EBPM practices could contribute to the robustness of IPM strategies available to grape growers.

Host Plant Associations of Anagrus spp. (Hymenoptera: Mymaridae) and Erythroneura elegantula (Hemiptera: Cicadellidae) in Northern California.

Anagrus erythroneurae S. Trjapitzin & Chiappini and Anagrus daanei Triapitsyn are the key parasitoids of the western grape leafhopper (Erythroneura elegantula Osborn) in northern California vineyards. Erythroneura elegantula overwinters as an adult in reproductive diapause. To successfully overwinter, Anagrus spp. must locate an alternate leafhopper host that overwinters in an egg stage that they can parasitize. These alternate leafhopper hosts are thought to be primarily located in the natural habitats surrounding vineyards. This study identifies the noncrop host plants utilized by Anagrus spp. not only during the overwintering period but throughout the entire year, as well as the leafhopper species associated with these host plants. Over a 2-yr period, Anagrus spp. and leafhoppers were sampled from numerous plants in natural and cultivated habitats surrounding vineyards. Results from this study confirm previously known Anagrus spp. host plants, but also identify new host plant species. Some of the host plants harbored Anagrus spp. year-round while others were utilized only during certain periods of the year. Leafhoppers associated with Anagrus spp. host plants may potentially serve as the alternate host utilized by Anagrus spp. on these plants, but this was not confirmed in the current study. Records of E. elegantula demonstrate their cyclical movement between the vineyard floor (winter), temporary noncrop hosts (spring/fall), and the grape vine canopy (summer).

Landscape Diversity and Crop Vigor Influence Biological Control of the Western Grape Leafhopper (E. elegantula Osborn) in Vineyards.

This study evaluated how the proportional area of natural habitat surrounding a vineyard (i.e. landscape diversity) worked in conjunction with crop vigor, cultivar and rootstock selection to influence biological control of the western grape leafhopper (Erythroneura elegantula Osborn). The key natural enemies of E. elegantula are Anagrus erythroneurae S. Trjapitzin & Chiappini and A. daanei Triapitsyn, both of which are likely impacted by changes in landscape diversity due to their reliance on non-crop habitat to successfully overwinter. Additionally, E. elegantula is sensitive to changes in host plant quality which may influence densities on specific cultivars, rootstocks and/or vines with increased vigor. From 2010-2013, data were collected on natural enemy and leafhopper densities, pest parasitism rates and vine vigor from multiple vineyards that represented a continuum of landscape diversity. Early in the season, vineyards in more diverse landscapes had higher Anagrus spp. densities and lower E. elegantula densities, which led to increased parasitism of E. elegantula. Although late season densities of E. elegantula tended to be lower in vineyards with higher early season parasitism rates and lower total petiole nitrogen content, they were also affected by rootstock and cultivar. While diverse landscapes can support higher natural enemy populations, which can lead to increased biological control, leafhopper densities also appear to be mediated by cultivar, rootstock and vine vigor.