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ARS Home » Pacific West Area » Wapato, Washington » Temperate Tree Fruit and Vegetable Research » Research » Research Project #430052

Research Project: New Technologies and Strategies to Manage the Changing Pest Complex on Temperate Fruit Trees

Location: Temperate Tree Fruit and Vegetable Research

2017 Annual Report


Objectives
This research will provide basic and applied information for the development and transfer of sustainable and environmentally acceptable methods and technologies for management of insect pests of temperate tree fruit crops. The objectives are: Objective 1: Develop new knowledge of the behavior, physiology, ecology, and biochemistry of insect pests and their natural enemies to suggest novel approaches to pest management and improve the use of existing methods, with focus on pest-host plant interactions of pear psylla and brown marmorated stink bug, pest-microbe interactions of codling moth and spotted wing drosophila, ecological and physiological criteria that limit pest distribution and abundance, and the functionality of codling moth receptors. Subobjective 1A. Determine and characterize interactions between pear trees and pear psylla and between the brown marmorated stink bug (BMSB) and preferred host plants. Subobjective 1B. Determine if volatiles emanating from microbial species found in the honeydew of aphids, mealybugs and psyllids are attractive to natural enemies. Subobjective 1C. Determine factors affecting pupal mortality and adult emergence of western cherry fruit fly (WCFF) in the field. Sub-objective 1D. Determine the upper and lower thermal limits for metabolism of different life stages of codling moth (CM), apple maggot (AM), and WCFF. Subobjective 1E. Develop a CRISPR/Cas9 gene knock out system to determine functions of proteins key to CM reproduction and development. Subobjective 1F: Determine undescribed cryptic species and undocumented range expansions of the community of minute pirate bugs in orchards and other habitats. Objective 2: Develop alternatives to fumigation to meet quarantine restrictions for pest insects in exported fruits, with focus on developing codling moth detector technology and ecological niche modeling to determine limits to the establishment and spread of quarantined insect pests. Subobjective 2A: Identify biochemical markers for apple fruit infested with CM larvae, in support of effort to develop detector technology. Subobjective 2B: Improve ecological niche models for the potential of tree fruit pests of quarantine concerns to establish and spread in potential new export markets. Objective 3: Develop and improve methods to reduce pesticide use and develop alternatives to pesticides, with focus on identifying and applying semiochemicals for pest management, and improved efficacy of natural enemies through application of foods and feeding attractants, and improvement of pear psylla control through induced or systemic acquired resistance in pear to psylla. Subobjective 3A. Develop an attract-and-kill approach for management of codling moth and leafrollers. Subobjective 3B. Improve efficacy of natural enemies through application of foods and feeding attractants. Subobjective 3C. Determine field temperature influences on the efficacy of the insecticide spinosad and Delegate for management of WCFF. Subobjective 3D. Improve pear psylla control through induced or systemic acquired resistance. Subobjective 3E. Evaluate the use of microbial-based feeding attractants for management of codling moth.


Approach
1A. Plant resistance to pear psylla will be characterized using greenhouse and biochemical assays and electrical penetration graphs. Host preferences by brown marmorated stink bug will be assessed by determining patterns of host plant use in non-crop landscapes. Stink bug attraction to host odor will be tested using a laboratory olfactometer. 1B. To develop methods of recruiting natural enemies to orchards, microbes present in aphid and pear psylla honeydew will be identified, and odors emanating from honeydew-associated microbes will be tested for attractiveness to natural enemies. 1C. Western cherry fruit fly adult emergence will be compared from soils with varying moisture and cover to determine whether fruit fly infestations in orchards can emanate from trees located in unmanaged habitats with dry soil surfaces. 1D. Data from differential scanning calorimetry and laboratory assays will provide estimates of metabolic thermal limits for codling moth, apple maggot, and western cherry fruit fly to determine the liklihood for these pests to establish and spread in new geographies. 1E. A CRISPR/Cas9 gene knock out system will be used to determine the function of proteins key to codling moth reproduction and development in support of work to develop species-specific behavioral and physiological modifying analogs for use in pest management. 1F. To improve conservation biological control in orchards, undescribed cryptic species and undocumented range expansions of minute pirate bugs in orchards and other habitats will be described based on morphometric analyses and molecular genetics. 2A. In support of efforts to develop technology to detect codling moth infestations in stored fruit, biochemical markers for infested apples will be identified using GC-MS, and laboratory studies will be used to determine how long marker chemicals are emitted from infested fruit. 2B. Experiments conducted in environmental chambers will be used to determine the effects of tropical and sub-tropical climates and photoperiods on the growth and development of codling moth, western cherry fruit fly, and apple maggot. Data will be used to improve ecological niche models for tree fruit pests of quarantine concerns to estimate the risk for these pests to establish and spread in export markets. 3A. New attractant blends will be developed as an attract-and-kill or mass trapping approach for management of codling moth and leafrollers. 3B. Plant-based attractive lures and food provisioning will be tested as attract-and-retain method of improving biological control in orchards. 3C. Effects of temperature on the efficacy of the insecticides Spinosad and Delegate for management of western cherry fruit fly will be determined using laboratory assays. 3D. Greenhouse assays and field studies will be used to test whether elicitors of host plant defenses can be used for the control of pear psylla. 3E. Laboratory studies will be performed to determine whether the addition of different yeast species with cane sugar stimulate codling moth feeding and increase the efficacy of ingested microbial or chemical insecticides against codling moth.


Progress Report
This progress report covers year two for the continuing project to develop and improve sustainable and biorational management and quarantine security of insect pests of temperate tree fruits. Key pests of concern include codling moth, pear psylla, spotted wing drosophila, apple maggot, and western cherry fruit fly. Substantial progress was made on all three objectives during this fiscal year. Brown marmorated stink bug (BMSB) is a recent introduction to the Pacific Northwest. There is little experience with managing this pest in the Pacific Northwest, and little understanding of this insect's threat potential, life history and population dynamics in the extensive areas of irrigated agriculture in the inland Northwest. Field sampling was continued for a second year to determine the incidence of BMSB, as well as native stink bugs on a set of native, weedy, and ornamental plants that are widespread in the Yakima Valley. This information generates hypotheses on hosts and preferred hosts of this recently introduced pest (Objective 1). Of note, Norway maple is now heavily used by BMSB in urban settings in eastern Washington. Additional laboratory assays demonstrated adult stink bug attraction responses to plant odors and to combinations of stink bug odor,pheromone, and plant odors. Pear psylla nymphs produce copious amounts of honeydew which causes fruit russeting, serves as a medium for the growth of sooty mold, and complicates harvest of pears. Scion wood taken from four pear varieties with resistance to pear psylla were grafted to rootstock and maintained in a greenhouse. To aid the development of new pear cultivars with insect resistance, these newly established trees will be used to identify mechanisms of resistance using stylet-pathway analyses and electronic penetration graphs. Field studies have been completed to determine whether defense elicitors used to control fire blight reduce populations of pear psylla. Results of these studies led to investigations to determine whether foliar antibiotics, also used for the control of fire blight, reduce endosymbionts of pear psylla and psyllid survival. A poor understanding of what shelter plants are most often used by overwintering psylla and cues that trigger overwintered psylla to return to pear orchards in spring complicates management practices targeting this bottlenecked population. Studies were initiated to develop a method using high-throughput direct sequencing for gut content analysis of pear psylla to identify which shelter plants are most suitable for overwintering psyllids. Winterform pear psylla were collected from shelter plants and pear orchards during winter and spring, and were stored at minus 80 degrees Celsius for gut content analysis after this new method is developed. To determine how winterform pear psylla locate pear trees in early spring, volatiles of budding pear trees were sampled and tested for evidence of attraction or aggregation by the insect. Understanding the role of natural enemies in orchards is made more complex with our realization that the natural enemy community in orchards and neighboring habitats includes species not previously known to occur in the Pacific Northwest. One important group of predators includes the minute pirate bugs, which are generalist predators of mites, psyllids, aphids, eggs and small larvae of caterpillars, and other soft-bodied arthropods. Almost 500 specimens of minute pirate bugs were obtained by loan from entomological museums in Canada, for use in updating northern distributions of native species. Additional specimens from ornamental plants were obtained from University of California, Riverside, to begin efforts at clarifying the taxonomically confusing mixture of species in Southern California and neighboring regions. Collecting efforts in Washington State and surrounding states are continuing. Specimens will be used to generate a list of external and anatomical traits that can be used to separate highly similar species. To reduce reliance on broad-spectrum pesticides, genetic control methods that are effective and environmentally sound need to be developed. One such method is to adapt clustered regularly-interspaced short palindromic repeats (CRISPR) CRISPR associated protein 9 (Cas9) genome editing for codling moth control. Two genes, one encoding an odorant receptor and one encoding a male dosage compensation protein, were edited with a CRISPR/Cas9 genome editing system optimized for use in codling moth. Experiments to determine the effects of genome editing of these genes were performed. These included polymerase chain reaction amplification and sequencing, high resolution melt analysis, flight tunnel bioassays, and mating assays. Four additional odorant receptor genes were characterized and sites to target with CRISPR/Cas9 genome editing were identified. Guide ribonucleic acids (RNAs) to target each gene were designed and production templates were generated through PCR and in vitro transcription. These guide RNAs will be used in gene editing experiments to be performed in the next year. Identification and improvement of chemical attractants and traps for moth pests will enable development of attract-and-kill management approaches, and improve monitoring using attractive lures. Studies were conducted to address several components needed to develop a successful, efficacious attract and kill approach for codling moth and leafrollers. Flight tunnel studies compared the effectiveness of different trap liners with captured females to lure additional males to the trap. Studies were conducted to develop a liquid method to catch moths in bucket traps that combines the use of organic oil, vinegar, and propylene glycol. The interaction of several aromatic volatiles with the sex pheromones of leafrollers were evaluated. Mass trapping studies are currently in place in commercial orchards. Further field comparisons of volatile blends for codling moth and leafrollers are being investigated. We are also characterizing the volatiles released by various microbes that are both present in various host plants and in shoots damaged by aphids and leafroller larvae. The microbiome will be characterized, prominent species will be cultured and identified, and volatile emissions will be collected in an attempt to develop new attractants for leafrollers. Western cherry fruit fly is abundant in unmanaged cherries in irrigated areas in the dry interior of the Pacific Northwest of the U.S. Irrigation may allow pupae to survive in soil during hot summers when risk of heat stress and desiccation is greatest. The hypothesis that western cherry fruit fly pupae survive better in irrigated than non-irrigated soils and grassy soils in a dry habitat in Washington State was tested. We added water or no water to soil or grassy soil (25 percent sand, 6 percent clay, and 69 percent silt) in pots embedded in the ground to simulate irrigation and no-irrigation schedules in a three-year study. Larvae were dropped into the pots for pupation. Simulated irrigation did not increase pupal survival before winter in soil, but it increased survival in grassy soil. In one of three years, adult eclosion rates in spring and summer also followed this pattern. While irrigation broadens the distribution of western cherry fruit fly by allowing host cherry trees to survive in dry habitats, natural precipitation in central Washington appears sufficient for pupal survival. Non-irrigated grassy soil appears most detrimental to pupal survival. Observations of larval behaviors and pupation success as well as predators in this environment could help explain this unexpected finding. To improve attract-and-kill approaches for western cherry fruit fly management, studies are testing the use of Spinosad and Delegate insecticides with sugar or yeast plus sugar for control of western cherry fruit fly. Relative efficacy of treatments will be determined based on numbers of adult flies caught on sticky yellow traps and by larval infestation of cherries. Temperatures in the orchard are being monitored using data loggers placed on trees around the periphery of the test plot. In the next two years, the same protocol will be followed using trees not used previously. Pest risk analyses estimate the risk that an insect pest will become established in export countries, and are used to define terms in export negotiations. Critical limits to growth and development of codling moth, western cherry fruit fly, and apple maggot were determined to improve pest risk analyses for these pests. Differential scanning calorimety was used to determine the upper and lower thermal limits of non-diapausing 4th and 5th instar, diapausing 5th instar codling moth, diapausing apple maggot, and western cherry fruit fly. Whole body supercooling points and total water content of apple maggot and western cherry fruit fly, and reduction of thermal tolerance of western cherry fruit fly was also determined. Total lipid, carbohydrate, and protein analyses for diapausing pupae apple maggot and western cherry fruit fly following various cold storage and rearing conditions have also been completed. Ecological niche models based upon accurate biological data are important for development of pest risk analyses. Ecological niche models were developed for western cherry fruit fly, codling moth, Oriental fruit moth, and apple maggot. Ecological niche models for western cherry fruit fly are being revised with physiological and ecological parameters for European cherry fruit fly. These revised models will assist the Animal and Plant Health Inspection Service in preventing the spread of this pest from Ontario, Canada, to commercial cherry productions areas in the United States.


Accomplishments
1. Knock-out of a pheromone receptor gene affects egg production and viability. The codling moth is a worldwide insect pest of apple and pear, and new methods that are safe and effective are needed to control it. ARS scientists in Wapato, Washington, used genomic technology to determine the function of an odorant receptor protein thought to be important in codling moth mating and reproduction. The gene encoding this odorant receptor was inactivated using clustered regularly-interspaced short palindromic repeats (CRISPR) CRISPR associated protein 9 (Cas9) genome editing. The results of this study revealed that inactivating this protein affected female codling moth's ability to lay viable eggs. Incorporating new strategies to inactivate this protein target in field populations will contribute to new and specific methods to control codling moth in the orchard.

2. An improved trapping system for Brown Marmorated Stink Bug (BMSB). The BMSB continues to spread, increase in numbers, and threaten a variety of crops. Improved detection and monitoring methods are needed to determine crop risks. ARS researchers in Wapato, Washington, in collaboration with scientists of Sterling International Inc. of Spokane, Washington, determined that a commercial pheromone lure deployed with a trap design used for paper wasps (TrapStik) yielded greater trap catches in comparison to pheromone-trap combinations currently in use. This development provides a more sensitive method of detecting Brown Marmorated Stink Bug populations.

3. Discovery of new biological control species in North America. The minute pirate bugs (Orius) are important sources of biological control in agricultural crops worldwide as predators of thrips, aphids, and mite pests. ARS scientists in Wapato, Washington, discovered that this group of predatory bugs in North America includes possibly four previously undescribed species which have been misidentified as one of our common described species. Specimens included one new species in agricultural regions of the Pacific Northwest, an undescribed species found in Southern California and Arizona feeding on thrips pests of ornamental plants, and possibly two undescribed species inhabiting native rangeland in Colorado and westwards into California, Oregon, and Washington. These results show that the minute pirate bug fauna in the Western U.S. is substantially more diverse than previously recognized, and that these predators are likely to contribute to biological control of a larger diversity of pest species than currently appreciated.

4. Defense elicitors suppress pear psylla populations. Pear psylla is the key insect pest of pear in the United States. This insect is primarily controlled using insecticides, and ongoing research seeks to discover new ways to manage this pest. Defense elicitors are foliar treatments which activate plant defenses leading to broad-spectrum immunity to numerous pests. ARS scientists in Wapato, Washington, tested the effects of three elicitors of plant defenses against pear psylla under field conditions. They found that the commercial elicitors, Actigard, Employ, and ODC, each reduce numbers of the damaging stage of pear psylla. These products are often used to control fire blight in pear orchards, and knowledge that these products reduce pear psylla will be useful for integrated pest management.

5. Development of gene editing using the codling moth maleless gene ortholog. Ribonucleic acid (RNA) interference has been useful for studying protein function in many insect species, however this technique is not very effective in lepidopteran insects, including the codling moth. ARS scientists in Wapato, Washington, developed clustered regularly-interspaced short palindromic repeats (CRISPR) CRISPR associated protein 9 (Cas9) gene editing technology for use in codling moth, a worldwide pest of apple and pear. The maleless gene ortholog was used as a model to develop and determine the effectiveness of CRISPR/Cas9 gene editing in codling moth. Optimizing egg injection techniques and timing, and guide RNA design led to a highly efficient gene editing system. Analysis of the deoxyribonucleic acid (DNA) sequences indicated that 85 percent of injected eggs exhibit genome modification of the targeted regions, and those modifications included both insertions and deletions. This success establishes our ability to perform the CRISPR/Cas9 genome editing in the codling moth.

6. Suitability of mango and other tropical and temperate fruit as hosts for apple maggot and cherry fruit flies. Apple maggot and western cherry fruit flies are quarantine pests of apple and sweet cherry, respectively, in the Pacific Northwest of the United States, but the flies have narrow host ranges that may reduce their threat to a wider range of fruit commodities. ARS scientists in Wapato, Washington, and scientists at Washington State University in Vancouver, Washington, tested the hypothesis that these flies do not utilize tropical fruit as hosts. In Washington, apple maggot flies infested only one percent of mangoes and zero percent of papayas hung in trees compared with forty-nine percent of apples. Cherry fruit fly infested only six percent of mangoes and zero percent of papayas versus thirty-three to seventy-three percent of cherry and plum in the laboratory. The low acceptability of mango and other tropical fruit provide evidence they would unlikely be attacked even if the flies were to be introduced into a tropical environment.

7. Impact of prolonged absence of low temperature on emergence patterns of western cherry fruit fly. The western cherry fruit fly is a quarantine pest of sweet cherries in the Pacific Northwest that is adapted to cold winters. The ability of this pest to establish and spread to markets in warm countries is affected by its ability to survive in warm temperatures. ARS researchers in Wapato, Washington, conducted a 3-year study to examine the effects of prolonged no chilling on fly emergence. It was found that a lack of chilling of diapausing pupae reduced the number of flies that emerged and delayed emergence times but did not completely prevent fly emergence. Results are important in that they can be used to develop revised models to predict fly emergence in warm climates.

8. Responses of snowberry and apple maggot flies to commercial and experimental sticky traps and odors. The apple maggot fly is a threat to the commercial apple industry in the Western U.S., requiring trapping surveys to detect its presence. A similar non-pest fly species, the snowberry maggot fly, is also caught on survey traps, increasing labor needed to process fly catches. ARS scientists in Wapato, Washington, and scientists at Washington State University, Vancouver, Washington, University of Notre Dame, Indiana, and Cornell University, New York, compared responses of the two flies to various traps and odors to identify best practices for reducing snowberry maggot fly captures in surveys. It was found that snowberry maggot flies responded more to sticky yellow rectangle than sticky red sphere traps, while the reverse was true for apple maggot flies. Snowberry maggot flies did not respond to apple odors attractive to apple maggot flies, but rather to snowberry fruit odors, while both species were attracted to ammonia odor. Our results are important in that they provide evidence that red spheres with apple or ammonia odor are better to use than yellow rectangles in apple maggot fly trapping surveys where snowberries are abundant.

9. Attraction of western cherry fruit fly to white light in the presence and absence of ammonia. Western cherry fruit fly is a quarantine pest of sweet cherry in the Pacific Northwest that can be detected using sticky yellow traps. Identifying factors that can increase the efficacy of traps baited with ammonia can be useful for improving fly management. ARS scientists in Wapato, Washington, determined if flies are attracted to white light from bulbs and whether light can be used to enhance fly captures in the field. In the laboratory, it was found that flies were attracted to bright white light in the presence and absence of ammonia odor. In the field, flies were not attracted to white light when ammonia odor was present, but they were when it was absent. Results are important in that they show responses to white light could partly explain fly behaviors and efficacies of traps.

10. Identification of host fruit volatiles from snowberry attractive to flies from snowberry in Washington State. Apple maggot fly is a pest of apples whose responses to fruit volatiles have been well studied, helping us understand the process of speciation in insects that attack plants. However, responses by a similar fly, Rhagoletis zephyria, to chemicals from host fruit have never been studied. ARS scientists in Wapato, Washington, and scientists at Cornell University in New York, University of Notre Dame in Indiana, Portland State University in Oregon, and Western Washington University in Washington, used gas chromatography and electroantennogram detection (EAD) to identify volatiles from the fruit of snowberry as key attractants for R. zephyria flies reared from snowberry fruit. A nine-component blend was identified that gave consistent EAD activity, and in a flight tunnel, snowberry flies displayed more flight to sources with snowberry than apple and hawthorn fruit volatiles. Findings provide evidence that differences among flies in their behavioral responses to host fruit odors represent key adaptations involved in host plant shifts.

11. Plant volatiles attractive to orchard moth pests. Discoveries of new attractive blends of plant volatiles for a diversity of orchard moth pests can allow improved pest management in these crops. ARS researchers in Wapato, Washington, found that two plant aromatics, when used with acetic acid, are effective attractants for both sexes of several leafroller species. It was discovered that either compound used in combination with a synthetic sex pheromone lure significantly reduces male catch compared with the pheromone alone. Adding acetic acid to these traps can increase the male catch to nearly comparable levels as the pheromone alone and allows female moths to be captured. This knowledge advances our development of lure and kill technologies for this important group of pests.

12. Collection of psyllid saliva. Salivary proteins have important roles in feeding by insects, but there are currently no published studies on the salivary proteins of psyllids. ARS scientists in Wapato, Washington, and Stillwater, Oklahoma, and scientists at Heritage University in Toppenish, Washington, developed methods to collect large quantities of salivary proteins from potato psyllid and pear psylla. These methods allow researchers to collect, identify and analyze salivary proteins of psyllid pests in pears and in other crops. This information leads to a better understanding of how psyllids feed and transmit plant pathogens.


Review Publications
Cooper, W.R., Garczynski, S.F., Horton, D.R., Unruh, T.R., Beers, E., Shearer, P., Hilton, R. 2017. Bacterial endosymbionts of the psyllid Cacopsylla pyricola in the Pacific Northwestern United States (Hemiptera: Psyllidae). Environmental Entomology. 46:393-402.
Cooper, W.R., Horton, D.R. 2017. Elicitors of host plant defenses partially suppress pear psylla (Cacopsylla pyricola, Hemiptera: Psyllidae) populations under field conditions. Journal of Insect Science. 17(2):49.
Beers, E., Horton, D.R., Miliczky, E. 2016. Pesticides used against Cydia pomonella disrupt biological control of secondary pests of apple. Biological Control. 102:35-43.
Beers, E., Mills, N., Shearer, P., Horton, D.R., Miliczky, E., Amarasekare, K., Gontijo, L. 2016. Nontarget effects of orchard pesticides on natural enemies: lessons from the field and laboratory. Biological Control. 102:44-52.
Giacomuzzi, V., Cappellin, L., Nones, S., Khomenko, I., Knight, A.L., Biasiolo, F., Angeli, S. 2017. Diel rhythms in the volatile emission of apple and grape foliage. Phytochemistry. 138:104-115.
Neven, L.G., Yee, W.L. 2017. Impact of prolonged absence of low temperature on adult eclosion patterns of western cherry fruit fly (Diptera: Tephritidae). Environmental Entomology. 46(3):708-713. https://doi.org/10.1093/ee/nvx064.
El-Sayed, A., Knight, A.L., Byers, J., Judd, G., Suckling, D. 2016. Caterpillar-induced plant volatiles attract conspecific adults in nature. Scientific Reports. doi:10.1038/srep37555.
Yee, W.L., Goughnour, R. 2017. Development of Rhagoletis pomonella and Rhagoletis indifferens (Diptera: Tephritidae)in mango and other tropical and temperate fruit in the laboratory. Florida Entomologist. 100(1):157-161.
Yee, W.L. 2017. Attraction of Rhagoletis indifferens (Diptera: Tephitidae) to white light in the presence and absence of ammonia. Florida Entomologist. 100(1):21-28.
Garczynski, S.F., Martin, J.A., Griset, M.L., Willett, L.S., Cooper, W.R., Swisher, K.D., Unruh, T.R. 2017. CRISPR/Cas9 editing of the codling moth (Lepidoptera: Tortricidae) CpomOR1 gene affects egg production and viability. Journal of Economic Entomology. 110(4):1847-1855.
Landolt, P.J., Cha, D.H., Zack, R.S. 2015. Synergistic trap response of the false stable fly and little house fly (Diptera: Muscidae) to acetic acid and ethanol, two principal sugar fermentation volatiles. Environmental Entomology. 44(5):1441-1448.
Kumar, S., Neven, L.G., Zhu, H., Zhang, R. 2015. Assessing the global risk of establishment of Codling moth (Cydia pomonella) using CLIMEX and MaxEnt niche models. Journal of Economic Entomology. 108(4):1708-1719.
Cha, D., Olsson, S., Yee, W.L., Goughnour, R., Hood, G., Mattsson, M., Schwarz, D., Feder, J., Linn, C. 2017. Identification of host fruit volatiles from snowberry (Symphoricarpos albus), attractive to Rhagoletis zephyria flies from Western United States. Journal of Chemical Ecology. 43(2):188-197.
Giacomuzzi, V., Mattheis, J.P., Basoalto, E., Angeli, S., Knight, A.L. 2017. Survey of conspecific herbivore-induced volatiles from apple as possible attractants for Pandemis pyrusana (Lepidoptera: Tortricidae). Pest Management Science. doi:10.1002/ps.4548.
Giacomuzzi, V., Cappellin, L., Khomenko, I., Biasioli, F., Schutz, S., Tasin, M., Knight, A.L., Angeli, S. 2017. Emission of volatile compounds from apple plants infested with Pandemis heparana larvae, antennal response of conspecific adults, and preliminary field trial. Journal of Chemical Ecology. 42:1265-1280.
Jones, V., Horton, D.R., Mills, N., Unruh, T.R., Miliczky, E., Shearer, P., Baker, C., Melton, T. 2016. Using plant volatile traps to develop phenology models for natural enemies: an example using Chrysopa nigricornis (Burmeister) (Neuroptera: Chrysopidae). Biological Control. 102:77-84.
Knight, A.L., Judd, G., Basalto, E. 2017. Development of 2-phenlethanol and acetic acid lures to monitor Obliquebanded leafroller (Lepidoptera: Tortricidae) under mating disruption. Journal of Applied Entomology. doi:10.1111/jen.12393.
Mills, N.J., Beers, E.H., Shearer, P.W., Unruh, T.R., Amarasekare, K.G. 2016. Comparative analysis of pesticide effects on natural enemies in western orchards: a synthesis of laboratory bioassay data. Biological Control. 102:17-25.
Unruh, T.R., Miliczky, E., Horton, D.R., Thomsen Archer, K.L., Rehfield-Ray, L.M., Jones, V. 2016. Gut content analysis of arthropod predators of codling moth in Washington apple orchards. Biological Control. 102:85-92.
Jones, V., Unruh, T.R., Horton, D.R., Mills, N., Brunner, J., Beers, E., Shearer, P. 2009. Tree fruit IPM programs in the Western United States: the challenge of enhancing biological control through intensive management. Pest Management Science. 65:1305-1310.
Landolt, P.J., Zhang, Q. 2016. The discovery and development of chemical attractants used to trap pestiferous wasps (Hymenoptera: Vespidae). Journal of Chemical Ecology. 42:7.
Cha, D.H., Adams, T., Landolt, P.J. 2017. Effect of chemical ratios of a microbial-based feeding attractant on trap catch of spotted wing drosophila (Diptera: Drosophilidae). Environmental Entomology. 46(4):907-915.
Derstine, N., Ohler, B., Jimenez, S., Landolt, P.J., Gries, G. 2017. Evidence for sex pheromones and inbreeding avoidance in select North America yellowjacket species (Hymenoptera: Vespidae). Entomologia Experimentalis et Applicata. doi:10.1111/eea12591.
Kumar, S., Yee, W.L., Neven, L.G. 2016. Mapping global potential risk of establishment of Rhagoletis pomonella (Diptera: Tephritidae) using MaxEnt and CLIMEX niche models. Journal of Economic Entomology. 109(5):2043-2053.
Yee, W.L. 2016. Ammonium carbonate loss rates from lures differentially affect trap captures of Rhagoletis indifferens (Diptera: Tephritidae) and non-target flies. The Canadian Entomologist. 149:241-250.
Yee, W.L., Goughnour, R.B. 2016. Peach is an occasional host for Rhagoletis pomonella (Walsh, 1867) (Diptera: Tephritidae) larvae in Western Washington State, USA. Pan-Pacific Entomologist. 92(4):189-199.