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Research Project: Improved Systems-based Approaches that Maintain Commodity Quality and Control of Arthropod Pests Important to U.S. Agricultural Production, Trade and Quarantine

Location: Commodity Protection and Quality Research

2021 Annual Report

The long-term objective of this project is to improve the quality of specialty crops grown in the western U.S. and increase their domestic consumption and export. All three objectives represent multiple, integrated issues focused on reducing insect damage, maintaining or improving quality and ensuring that exported commodities meet all phytosanitary requirements. Project integration will facilitate successful implementation of systems-based control strategies into current crop production systems, delay the development of resistance to chemicals used for control or disinfestation, overcome trade barriers for the export of fresh fruits and nuts, and minimize deleterious effects of these chemicals on the environment. Objective 1: Develop new or improved preharvest processes that are acceptable to industry and regulatory partners that reduce the incidence of pests in fresh and durable commodities prior to harvest. Sub-objective 1A: Improve current integrated pest management strategies for control of navel orangeworm (NOW) in order to reduce damage and minimize nontarget impacts on environmental quality. Sub-objective 1B: Reduce NOW damage to almond and pistachio orchards by characterizing the environmental and host factors associated with high NOW damage to orchards and develop strategies to eliminate them or mitigate their impact. Sub-objective 1C: Minimize chemical treatment requirements by characterizing and optimizing integrated pest management strategies for monitoring and control of key dipteran and lepidopteran pests. Sub-objective 1D: Improved management of pests of high-value commodities through generation of molecular resources and development of genomics-based approaches. Objective 2: Develop new or improved postharvest processes for the control of arthropod pests, such as handling procedures and treatments, that contribute to food security and food safety while maintaining commodity quality. Sub-objective 2A: Improve semiochemical-based strategies for control of stored product insect pests. Sub-objective 2B: Develop novel postharvest treatments for fresh and durable commodities that maintain or improve commodity quality while protecting the commodity against arthropod pests. Sub-objective 2C: Improve the sustainability of methyl bromide alternatives using molecular toxicology approaches to understand pest physiology, in the context of emergence of insecticide resistance. Objective 3: Ensure that new treatments comply with environmental, human health, sanitary, and phytosanitary regulations, including local, state, national, and international regulations. Sub-objective 3A: Develop treatments for action agencies and industry that satisfy the regulatory requirements of the exporter and importer, ensuring that technology implementation results in market retention or expansion. Sub-objective 3B: Identify agrochemical use strategies and develop novel technologies to ensure residues are compliant with importer and domestic food tolerances. Sub-objective 3C: Develop technologies that reduce or eliminate atmospheric emissions during ventilation of postharvest fumigations to address air quality criteria.

This project has one overarching theme, maintaining or improving the quality of west coast horticultural commodities in order to maintain or expand market share, by improving existing systems approaches and developing new ones. This complex project contains three objectives, 10 sub-objectives, and 13 research goals. The research focus of Objective 1 is preharvest, and three sub-objectives and four research goals target the navel orangeworm (NOW), the primary moth pest of California tree nuts. Research will evaluate the feasibility of a nonchemical alternative, sterile insect technique and facilitate the integration of another nonchemical technique, mating disruption, into existing management programs. These programs will be improved by enhancing the efficacy of existing insecticides through changes in timing and improvements in coverage, as well as recognizing orchards at increased risk for damage. The final NOW sub-objective determines the feasibility of using RNAi-mediated reduction in target gene expression to improve its control, as well as that of citrus red scale. The final sub-objective in Objective 1 seeks to improve the monitoring and control of dipteran pests such as the spotted wing drosophila, the Mediterranean fruit fly, and the melon fly, by improving existing attractants and developing new ones. The research focus of Objective 2 is improved control of coleopteran and lepidopteran pests of fresh and durable commodities in storage. It contains three sub-objectives and four research goals. The first sub-objective and two research goals are far ranging and involve novel methods to synthesize semiochemicals and develop new methods to dispense them. Additional studies seek to improve mating disruption using the same semiochemicals for both disruption and detection. The final two sub-objectives and two research goals are independent but related to one another. One sub-objective is quite broad; developing novel postharvest treatments for fresh and durable commodities. The control methods assessed include low oxygen controlled atmosphere, cyanide, sulfuryl fluoride, phosphine, and ethyl formate, alone and in combination, as well as irradiation. The focus of the final sub-objective is to identify the insect genes responsible for both ethyl formate toxicity and the combination of ethyl formate and CO2 used as an additive, in brown marmorated stinkbug, in order to improve control. The research focus of Objective 3, which contains three sub-objectives and four research goals, is to ensure that the techniques and technologies developed in the earlier objectives can be adopted. The first sub-objective and research goal ensures that treatments developed for lepidopteran and dipteran pests are in compliance with all pertinent regulations. The second sub-objective and two research goals focuses on generating efficacy and residue data to support the use of ethyl formate and sulfuryl fluoride as substitutes for methyl bromide. The final sub-objective and research goal focuses on developing recapture technologies to reduce or eliminate fumigant emissions into the atmosphere.

Progress Report
This is the first report for project 2034-43000-043-00D, “Improved Systems-based Approaches that Maintain Commodity Quality and Control of Arthropod Pests Important to U.S. Agricultural Production, Trade and Quarantine,” which began on 12/07/2020. This project replaced bridging project 2034-43000-042-00D, “Systems-based Approaches for Control of Arthropod Pests Important to Agricultural Production, Trade and Quarantine.” In support of Sub-objective 1A, a series of field trials were conducted to determine if the water volume used for insecticide application in pistachios could be reduced from 100 gallons per acre to 50 gallons per acre using organosilicone adjuvants. Trials conducted after July 14, 2020, used 50 gallons of water per acre at an adjuvant concentration of 0.1% added to an insecticide containing methoxyfenozide. Based on the results of contact toxicity bioassays, this concentration provided a duration of control of two weeks. This was the first positive outcome at this reduced water volume, but in pistachios the duration of control needs to be at least three weeks. Future trials will evaluate the combination of organosilicone adjuvant and 70 gallons of water per acre applied using airblast sprayers. Air application was also assessed and increasing the concentration of organosilicone adjuvant did not extend duration of control when 15 gallons of water per acre were applied. These experiments will be repeated in 2021 in order to determine the most efficacious concentration of organosilicone adjuvant to pair with choice of application (ground versus air). In support of Sub-objective 2B, colonies of three species of flat mite Tarsonemus bakeri, Brevipalpus californicus and B. lewisi were established with cooperation from the University of California Kearney Research Center. These three species are major pests of California citrus and avocados. Efficacious postharvest treatments are critically required, as fumigations and cold treatments are ineffective for a variety of reasons, ranging from a lack of toxicity to unreasonable requirements, such as taking too long or being too expensive for industry. To support treatment development, populations were collected in Exeter, California, transferred to the lab, and reared on Valencia oranges in an incubation chamber. For identification, 10 females of each species were observed under a compound microscope with oil emersion and species identification determined using taxonomic keys. Research planned for 2022 seeks to evaluate novel approaches, including the use of surfactants and ethyl formate. In support of Sub-objective 3A, colonies of Asian citrus psyllid (ACP), Western cherry fruit fly (WCFF), blueberry maggot (BBM), and Mexican fruit fly (MFF) were established, with USDA Animal and Plant Health Inspection Service permitting, inside the Contained Research Facility (CRF) at the University of California, Davis. All of these species are managed by quarantines, so many precautions and regulations are required to establish populations. An ACP population was sourced from a CRF cooperator who maintains a vigorous colony production system. WCFF was sourced from ARS in Wapato, Washington, by a cooperator who supplies field collected pupae once a summer. Similarly, BBM pupae are shipped from Southwest Michigan each summer. WCFF and BBM are reared on sweet cherries and blueberries, respectively, allowing relevant access to all life stages of these flies. MFF are sourced approximately every three months from USDA in Mission, Texas, and reared on mandarin oranges for testing purposes, or corn cobb diet for propagation. The research planned for 2022 seeks to evaluate novel postharvest approaches for insect control. In support of Sub-objective 3C, research was conducted to evaluate ways to minimize or eliminate fumigant from the ventilation effluent. Environmental regulators are concerned at the international- (Montreal protocol) and federal-levels (Clean Air act) about these emissions. Authorities, in several cases, have elected to mandate recovery and recycling technologies. By outfitting the chamber ventilation stream with a bed containing activated carbon (AC), atmospheric emissions can be greatly reduced. A testing scheme, previously developed and published by the ARS, was used to quantitatively evaluate the sorption potential for sulfuryl fluoride (SF) and ethyl formate (EF), two key methyl bromide alternatives. SF was only minimally sorbed by the AC, indicating poor potential for this strategy. EF, however, was strongly sorbed, and in fact appreciably hydrolyzed, by AC. Research planned for 2022 will explore its commercial potential at the pilot scale.

1. Determining the mechanism of pyrethroid resistance in navel orangeworm. The navel orangeworm is the most important insect pest of the $8 billion dollar almond and pistachio tree nut industry in California and is currently controlled by a combination of sanitation, insecticide application, and mating disruption. Pyrethroid insecticides are heavily used because of their efficacy combined with low cost. An ARS researcher in Parlier, California, working with collaborators at the University of Illinois at Urbana-Champaign, found that pyrethroid resistance (as high as 110-fold) primarily results from increased expression of mixed function oxidases belonging to the P450 family. Additionally, resistant navel orangeworm adults had a thicker epicuticle and their eggs had a thicker shell. This finding is important because this increased thickness may provide protection from insecticides belonging to other families. This finding underscores the need for coordinated management strategies to delay insecticide resistance.

2. Control invasive and quarantine horticultural pests. ARS researchers in Parlier, California, conducted studies to optimize, develop, and register methyl bromide (MB) alternatives to support regulatory compliance and enhance global food security. The research directly resulted in market retention or expansion and served as the basis for technical interaction between industry, USDA Foreign Agricultural Service, USDA Animal and Plant Health Inspection Service, U.S. Environmental Protection Agency, and respective counterparts in foreign governments. The researchers developed a novel postharvest phosphine fumigation to control spotted wing drosophila (SWD) in fresh citrus exports from California to New Zealand, valued at $12 million annually. In addition, a novel postharvest sulfuryl fluoride fumigation was developed to control navel orangeworm, almond moth, and Mediterranean flour moth in almond exports from California to India, valued at $2 billion annually.

3. Limiting the possible negative impact of postharvest fumigation. ARS researchers in Parlier, California, conducted studies to enhance the understanding of how fumigants impact human and environmental health. Research on off-gassing potential and labeling of postharvest fumigants, including methyl bromide (MB), phosphine, propylene oxide, sulfur dioxide, and ethyl formate (which are used to treat U.S. horticultural goods valued at approximately over $50 B annually) critically supported mandatory reviews by California and the U.S. Environmental Protection Agency regarding applicator, worker, by-stander, and consumer exposure. Sulfuryl fluoride (SF) is a key MB alternative that is used around the world to treat durables, such as tree nuts and logs. The five largest ports in the European Union and Australia have demanded that SF emission be curtailed due to its greenhouse gas potential. In late fall of 2020, ARS researchers in Parlier, California, developed a commercial scrubbing technology that is now in widespread use. This research should help preserve the use of SF across the globe and reduce greenhouse gas levels.

Review Publications
Higbee, B.S., Burks, C.S. 2021. Individual and additive effects of insecticide and mating disruption in integrated management of navel orangeworm in almonds. Insects. 12(2):188.
Walse, S.S., Jimenez, L. 2021. Postharvest fumigation of fresh citrus with cylinderized phosphine to control bean thrips (Thysanoptera: Thripidae). Horticulturae. 7(6):134.
Zhao, C., Liao, P., Miao, S., Nabity, P., Bansal, R., Liu, C. 2021. Tripartite parasitic and symbiotic interactions as a possible mechanism of horizontal gene transfer. Ecology and Evolution.
Hausch, B.J., Arpaia, M., Kawagoe, Z., Walse, S.S., Obenland, D.M. 2020. Chemical characterization of two California-grown avocado varieties (Persea americana Mill.) over the harvest season with an emphasis on sensory-directed flavor analysis. Journal of Agricultural and Food Chemistry. 68(51):15301-15310.
Demkovich, M.R., Calla, B., Ngumbi, E., Higbee, B.S., Siegel, J.P., Berenbaum, M.R. 2021. Differential regulation of cytochrome P450 genes associated with biosynthesis and detoxification in bifenthrin-resistant populations of navel orangeworm (Amyelois transitella). PLoS ONE. 16(1). Article e0245803.
Sirot, L., Bansal, R., Esquivel, C.J., Arteaga-Vazquez, M., Herrera-Cruz, M., Pavinato, V.A., Abraham, S., Medina-Jiménez, K., Reyes-Hernández, M., Dorantes-Acosta, A., Pérez-Staples, D. 2021. Post-mating gene expression of Mexican fruit fly females: disentangling the effects of the male accessory glands. Insect Molecular Biology. Available:
Haviland, D.R., Rijal, J.P., Rill, S.M., Higbee, B.S., Gordon, C.A., Burks, C.S. 2021. Management of navel orangeworm (Lepidoptera: Pyralidae) using four commercial mating disruption systems in California almonds. Journal of Economic Entomology. 114(1):238-247.
Bansal, R., Mian, R.M., Michel, A. 2021. Characterizing resistance to soybean aphid (Hemiptera: Aphididae): antibiosis and antixenosis assessment. Journal of Economic Entomology. 114(3):1329-1335.