UNDERSTANDING AND MANAGING ARTHROPOD PESTS, NATURAL ENEMIES AND POLLINATORS THROUGH ECOLOGICALLY-BASED INTEGRATED PEST MANAGEMENT APPROACHES ON TREE FRUITS IN PENNSYLVANIA.

• Sponsoring Institution: National Institute of Food and Agriculture
• Project Status: COMPLETE
• Funding Source: HATCH
• Reporting Frequency: Annual
• Accession No.: 1011647
• Project Start Date: Feb 2, 2017
• Project End Date: Dec 31, 2021
• Program Code: [(N/A)]- (N/A)

Project Director
Biddinger, DA, J.

Recipient Organization
PENNSYLVANIA STATE UNIVERSITY
208 MUELLER LABORATORY
UNIVERSITY PARK,PA 16802

Performing Department
Entomology

Non Technical Summary
Long-term stailibity of fruit agro-ecosystems is the ultimate goal of this project. While significant advances have been made in the past decade towards moving to ecologically-based IPM as mandated by the National IPM Roadmap and promoted by the Food Quality Protection Act, the stability of tree fruit IPM in Pennsylvania and other mid-Atlantic states is threatened by: the introduction of invasive species such as BMSB and SWD; the elimination of older insecticides through regulatory action; pesticide resistance development in key pests such as codling moth, Oriental fruit moth, and European red mite; and the effects of a plethora of newly registered insecticides/miticides with novel modes of action that often have sublethal reproductive effects on beneficial insects and pollinators. The goal of this project is to develop new information on the behavior, phenology, and control tactics for selected pests that will provide the basis for a safer work environment of tree fruit IPM programs. To obtain this goal specific research objectives are given.

Animal Health Component

70%

Research Effort Categories

Basic

20%

Applied

70%

Developmental

10%

Classification

Knowledge Area (KA)	Subject of Investigation (SOI)	Field of Science (FOS)	Percent
211	3120	1130	100%

Knowledge Area
211 - Insects, Mites, and Other Arthropods Affecting Plants;

Subject Of Investigation
3120 - Spiders, mites, ticks, and other arthropods;

Field Of Science
1130 - Entomology and acarology;

Keywords

integrated pest management

pollinator conservation

biological control

pesticide effects

solitary bees

neconicotinoid toxicity

Goals / Objectives
1. To assess the toxicity (e.g., acute, chronic and sublethal) of experimental and registered insecticides/acaricides, bacterial and viral pathogens, in laboratory, greenhouse, and orchard experiments towards populations of economically important arthropod pests, with special consideration for their effects on natural enemies and pollinators, their propensity for resistance development, and their compatibility with sustainable integrated pest management programs in both conventional and organic orchards.2. To evaluate, understand and integrate the various methods of employing sex pheromone mating disruption into an overall management approach for the major lepidopteran pests of deciduous tree fruits and to determine the economic feasibility of mating disruption on general insecticide usage, outbreaks of secondary pests, natural enemies and as a means to manage insecticide resistance.3. To investigate the biology, behavior, movement and management of historical and invasive pests (i.e., BMSB and SWD) on apple, peach and cherry to understand and elucidate the factors influencing their development, behavior, induction of diapause, and movement of adults among and between various host crops.4. To develop and validate predictive degree-day models and practical sampling plans for estimating the correct timing to employ various management approaches and to determine the relative density and incidence of various pests in order to minimize the potential for pests to cause economic injury to deciduous tree fruit crops.5. Determine the diversity, utility, and means to conserve native bees and honey bees as pollinators of fruit crops and integrate pollinator conservation into current IPM fruit systems.

Project Methods
Objective 1: Both experimental and registered insecticides and acaricides will be evaluated in replicated laboratory bioassays and/or orchard experiments for their potential or continued use as valuable tools for both IPM and organic programs. Products will be evaluated to determine their mode of action, speed of kill or feeding effects, and efficacy at various concentrations and timings on the many different pests attacking deciduous tree fruits as well as their toxicity towards natural enemies of this complex. Previously published methods (9) will be used for collecting records on foliage, fruits and other parts of the tree in evaluating these materials for prevention of injury and possible phytotoxic effects. Data will be assembled on the ability of natural enemies to survive and reproduce under various management programs. Special attention will be given to determining optimal concentration, method of application, timing and interval between applications in order to maximize survival of natural enemies and minimize resistance development in pests. Standardized bioassay procedures to monitor for the development of insecticide/acaricide resistance both in the laboratory and orchards will be used for a number of pests, especially codling moth, Oriental fruit moth, spider mites and BMSB.Objective 2: Studies involving various application technologies (e.g., sprayable formulations, attract and kill, hand-applied dispensers, puffers, etc. for both single and multiple species) to dispense sex pheromone for mating disruption will be conducted in a number of large orchard blocks for a variety of species, but in particular the codling moth and Oriental fruit moth. Orchards with a range of pest densities will be used. At each orchard site a minimum of two treatments will be assigned to relatively isolated blocks of at least 4-8 hectares each, a pheromone treatment and a conventional insecticide program. If possible, a third treatment of an isolated small section will receive neither pheromone nor insecticide to serve as an untreated control. Growers will utilize standard management practices in all conventional blocks. In the mating disruption blocks insecticides will be withheld unless the targeted pests exceed their economic injury levels or if needed, they will be timed according to degree-day based recommendations. Sex pheromone and kairomone traps for all targeted pests will be monitored throughout the season to determine relative pest pressure and trap shut down by the pheromone source. Fruit injury will be determined after each pest brood to monitor success during the study and again at harvest. Data on the status of non-targeted pests (e.g., aphids, leafhoppers, mites, etc.) and natural enemies in the orchard will be taken at each treatment site. For the long-term studies (i.e., 3-5 years) larvae from each mating disruption and conventionally treated site will be collected through time and evaluated using standard bioassay techniques to assess the stability of insecticide resistance. Insecticide schedules and the achieved value of the fruit from each treatment block will be collected from the growers and an economic analysis will be run comparing mating disruption to conventional insecticide use.Objective 3: Laboratory and field studies will be designed to investigate host plant effects on the population dynamics and behavior of various fruit pests including invasive species and some species of bee. Field investigations involving regular collection of juvenile stages and adult pests at weekly intervals during the season on both apples and peaches will help to determine the developmental status of various pest populations. Further sampling for BMSB eggs on both apple and peach will help develop models for egg hatch phenology and also shed light on questions related to ovipositional preference between hosts, and between various sites within given host plants. Mark-release-recapture studies will be implemented to study pest and bee dispersal and movement within and between orchards. Pests be reared from laboratory colonies and marked with fluorescent powders of different colors or with an immunoassay technique using egg proteins. They will be released in commercial orchards of both apple and peach plantings with each planting at least 8-10 acres in size. Portable weather stations at each site will be used to collect data on wind speed and direction, air temperature, and humidity. Field data will be analyzed with a variety of statistical techniques to assign significance to differences between variables in the experiments, and to make conclusions about the biological relevance of the findings.Objective 4: Phenological predictive models relating egg hatch to degree-day accumulations will be developed and validated for each pest species monitored and for the solitary bee, Osmia cornifrons. These models will be incorporated into PAPipe, a web-based Geographical Information tool that will inform growers about pest development on their farms. Intensive sampling experiments will be conducted to gather data on the temporal and spatial dynamics of several important pests and pollinators. Within-tree and orchard stratified sampling procedures; appropriate leaf, fruit and pheromone trap catches will be utilized to estimate the variance components that describe the change in pest numbers among habitat units. Sampling plans will then be constructed that give the most precise estimates of population parameters for a given level of precision and cost in terms of time and labor.Objective 5: In cooperation with the Pennsylvania Department of Agriculture, we will survey pollinators by net collection, timed counts and colored pan traps in a number of apple orchards managed with RR IPM or conventional IPM to determine the impact of pesticides on bee diversity and ecology. Bioassays on honey bees and Osmia sp. (as a representative of pollen bees) will be conducted to determine the comparative toxicity of various insecticides and fungicides. To determine the shorter foraging ranges of some of the pollen bees, an protein immunoassay technique will be used to mark bees with a protein and then collect fruit flowers at known distances from a nest to determine the range and frequency of visits during bloom. Horticultural measures of fruit set, fruit quality and yield will be taken in six apple orchards that are relying on pollen bees only for pollination to determine the effectiveness over distance from nesting habitat adjacent to orchards of wild pollinators. In conjunction with USDA-NRCS and the Xerces Society, the use of pollinator strips will be evaluated in fruit orchards to determine if they supplement forage for fruit pollinators, provide shelter from pesticides, and provide habitat for short-ranged bees to fly into the centers of larger orchards. Tactics for Osmia bees will be developed to determine if they can be managed like honey bee colonies to supplement or replace honey bees for pollination needs.

Progress 10/01/19 to 09/30/20

Outputs
Target Audience:Target audiences include the 450 fruit growers in Pennsylvania and equivalent numbers in the adjacent mid-Atlantic fruitgrowing regions of Delaware, Maryland, Virginia, West Virginia, New York, New Jersey, and North Carolina. Many presentations have been made at professional meetings to peer scientists, government officials, pesticide industry, and policy makers in various agencies within USDA, including Animal and Plant Health Inspection Service, Natural Resources Conservation Service, Agricultural Research Service, and National Institute of Food and Agricuture, as well as the Environmental Protection Agency. The public has been engaged through large field days at the PSU Research Station, through workshops with the Xerces Society and PASA (PA Sustainable Agriculture) and several on-line publications through the NE IPM centers, Penn State Extension, Penn State Center for Pollination, Research, USDA-NRCS publications, and the Xerces Society website. Changes/Problems:The biggest change/problem in 2020 was of course the Covid 19 pandemic which greatly restricted travel and the ability to hire summer help and the daily routine of faculty and support staff technicians that normally support these programs. Those faculty at the Fruit Research and Extension Center were designated as essential workers early on, so worked throughout the pandemic, but withlimited help. Travel to conduct SLF research required weekly permission and was restricted to a single person per vehicle, with no overnight stays in hotels. Although we continued to advise fruit growers on-line and by phone, personal interactions such as farm visits were eliminated and extension meetings were conducted mostly on-line. Several graduate students were caught overseas when Covid 19 hit and are still not able to return to the US to resume research or defend their thesis for an indefinite period. Several thesis defenses planned for this year have been delayed or conducted remotely. Conference presentations of research have been either cancelled or have gone on-line. Those with teaching responibilities have had to develop on-line courses and those with children in school are also working as teachers or filling the role of day-care in the past. Possible lay-offs in the future also contribute to additional stress as do concerns over the health of older relatives and children being exposed by in-person classes. Spotted Lanternfly has become such a significant economic pest on grape and political quarantine problem that the focus, time and resources of Biddinger and Krawczyk has been increasingly taken away from normal fruit IPM to developing control tactics for this pest. This comesat the expense of further developing IPM programs and tactics for controlling tree fruit pests and conserving beneficial arthropods and pollinators. We now cover to some extent, grapes and forestry research and extension and are dealing with state and national government agencies on SLF policy. SLF basic research has to be conducted within the quarantine facilities at the PSU main campus or in a USDA facility in Maryland.Conducting SLF research within the quarantine zone is difficult as it is three hours from the PSUcampus and two hours from the Fruit Research and Extenson Center in Biglerville. Getting 50% of a technician's time at thePSU Berks campus and the hiring of an extension associate to work on SLF within the quarantine has greatly increased productivity and reduced road travel time. As pesticide companies continue to consolidate through mergers and experience financial difficulties, grant in-aid for pesticide testing is becoming more unpredictable and it is becoming more difficult to maintain research orchards and personnel for this type of research. What opportunities for training and professional development has the project provided?A total of 71 undergraduates, 12graduate students, and two post-doctoral scholars were trained in various aspects of pollinator ecology and toxicology, invasive species biology and control, and IPM in tree fruit and grapes. In 2020, two students graduated with aPh.D. in ecology or entomology. A full-day, hands-on workshop trained 25 extension educators, bee keepers and Master Gardeners in advanced bee identification, bee conservation techniques, and IPM techniques to minimize pesticide impacts at the mid-Atlantic Fruit and Vegetable Conference inHershey, PA. How have the results been disseminated to communities of interest?Over 50 extension presentations have been made to fruit growers, bee keepers, and the interested public. Several fact sheets on various aspects of SLF biology and control are available to the public at the PSU extension website. Dozens of interviews to trade journals, newspapers, and government agencies have been made on-going SLF research and control efforts for tree fruit pests and conserving biological control of secondary pests. Several dozen peer-reviewed publications have informed the scientific community, as well as departmental seminars and presentations at professional societies. Tree and small fruit growers, government agencies, and homeowners receive updated recommendations on pesticide impacts and conservation of both honey bees and native bees as well as biological control agents of pests in the revised 2020-21 edition of the Penn State Tree Fruit Production Guide. This award winning guide has always been available on-line and is considered one of the most complete and effective guides of its type in the US and is internationally recognized. The concept of integrating pollinator protection into IPM was proposed in a publication by Biddinger & Rajotte and has now been accepted by the Entomological Society of American's Pollinator Health Position Statement and in several USDA grant programs including SCRI and AFRI and so have reached a much larger audience than just tree fruit growers. Publication with the Xerces Society have reached far beyond the 2% of the population that are farmers, but are now influencing the general public with over 100,000 downloads on the "How Neonicotinoid Insecticides Can Kill Bees" review series and technical manuals with USDA-NRCS on pollinator wildflower plantings and perennial hedgerows are informing many other agricultural crops and regions than just the mid-Atlantic states. The IPM concept is taught in IPM graduate courses and extension workshops at Penn State by Rajotte, Lopez-Uribe and Biddinger, as well as winter extension presentations to fruit growers and Master Gardeners. What do you plan to do during the next reporting period to accomplish the goals?Collaborators will 1) perform research on Spotted Lanternfly (SLF) addressing questions bridging a range of applied to basic aspects of SLF biology, and 2) integrate results from research findings into a strategic management plan of SLF that provides short-term immediate solutions to the current danger of SLF in Pennsylvania, and sustainable long-term solutions to mitigate SLF spread and damage to other locations within the US. We will continue to evaluate new and registered insecticides for tree fruit pests, develop bettter methods for monitoring and timing of insecticide interventions while trying to conserve pollinators and biological control agents of secondary pests such as mites, scale, and aphids.

Impacts
What was accomplished under these goals? Objective 1 (Biddinger & Krawczyk).Resistance in codling moth, due tosome control failures in Fruit Research and Extension Centertrials over the last couple of years, have prompted increased testing of alternative products toDelegateas rotation partners to the diamide Altacorand the initiation of laboratory bioassays toquantify resistance levels. We continue to evaluate in our experimental orchards on station any newinsecticides being developed by various agrichemical companies, but mergers of several of these companies have put a holdon development of new products withEnkounteras the only product being registered recently. Several experimental miticides were evaluated for efficacy and compatibility with predator mites. Objectives 1 and 3 (Krawczyk). Evaluations of long-lasting insecticide treated nets to manage brown marmorated stink bug (BMSB) and spotted lanternfly (SLF) are intiallyverypromising. The same net as deployed against BMSB, is also effective in killing SLF, however the lack of effective SLF attractant makes this method less useful for this pest. The activities under the United States Agency for International Development (USAID) Restoring Efficency in Agriculture Program (REAP)in the Republic of Georgia resulted in the development of national BMSB management program, which is generally based on the alternative management of BMSB. Objectives 1 and 4 (Biddinger). Control measures for San Jose Scale (SJS) are now shifting more to controlling the immature SJS crawlers post-bloom rather than trying to suffocate overwintering adults with oil. To this end, we are trapping SJS adult males with pheromone traps and refininga degree day model for precise timing of sprays forthe susceptible crawlers. The SJS pheromone lure is also very attractive to the main biological control wasp,Encarsia perniciosi, which we are also monitoring to determine periods of vulnerability to pesticides in order toconserve them. Currently, SJS sprays are prophylactic and based mostly on the presence of fruit injury the previous season, so we are evaluating new thresholds based on SJS male trap catch andparasitoid/prey ratios. At least a dozen insecticides have been evaluated for SJS control pre- and post-bloomand are also evaluated to see if they will work on other summer fruit pests. Objectives 1 and 5 (Biddinger, Krawczyk, Lopez-Uribe, & Grozinger). We continue to test pesticides on tree fruit pests, but additionally have been determining field realistic doses in nectar and pollen when they are applied pre-bloom to petal fall and are finding some fungicides to be much more toxic to bees than previously thought. In trials comparing honey bee susceptibility to Osmiabees, we have found Osmia to generally be much more susceptible to both insecticides and fungicides than the honey bee. This work is being conducted by two Ph.D. students and much of it will be published in the next 6 months. An M.S. student started this summer to evaluate the effect of SLF insecticide sprays in forestry and fruit crops to pollinators, beneficial insects and other non-targets. Long-term bee monitoring studies to look for pollinator declines since 2009 continue with approximately 150,000 bees and 17, 000 syrphid flies having been collected to date representing over 265bee species and 40 syrphid species found in apple and cherry orchards. We have changed apple pre-bloom insecticide recommendations for neonicotinoid applications to reduce insecticide levels found in the nectar and pollen and only recommend two of the safest neonicotinoid insecticides out of the sevenregistered. Werecommend Beleaf (flonicamid) as a beesafealternative for RAA control pre-bloom as late as the pink stage. Additionally, we are evaluating the effects of commonpre-bloom and bloom fungicides on both the honey bee and Osmia and found some products to be much more toxic to Osmia.Lipid/protein ratios of various pollen sources have been examined in both the honey bee and Osmia cornifrons to better understand the optimal diet and floral resource plants needto conserve or augment both types of bees for fruit growers. Objective 2 (Biddinger & Krawczyk). Mating Disruption research has been reduced as invasive pests such as SLF, Spotted Wing Drosophila, and BMSB have resulted in the need for more traditional contact and systemic insecticides than before, leaving expensive, target specific pheromone mating disruption at a major disadvantage in cost, so that the use of mating disruption in orchards has declined. Pheromone research is now concentrating on finding compounds attractive to BMSB and SLF that can be used for monitoring populations, but none of the products have proven to be effective enough for large scale mating disruption, especially since both of these pests mostly mate outside of orchards in the local landscape and then move into orchards already mated. Objective 3 (Biddinger & Rajotte). Evaluations of the bioinsecticides and organic products such asBeauveria products, essential oils, azadiractin, and long-chain soap productsare being evaluatedfor SLF control in agricultural crops, ornamental nurseries, and forests. SLF control has been better in both large scale plots and on potted trees and vines than originally thought and different formulations and application methods are being examined toimprove efficacy and residual, includingan ultra-low volume formulation for aerial applications. Objectives 3 and 4 (Biddinger & Krawczyk).Approximately 50 insecticides have been evaluated for contact and residual activity on SLFadults and nymphs at both grape and peach label rates. From these trials, 15 insecticides have had 2e label amendments to add SLF to the list of pests that each compound will control. Without this, applications for SLF would be off label and would be "targeting other late season pests,"so that product failures would not be covered by the manufacturer. Many products were found to be effective on SLF, but long residual activity reducingthe number of applications has to be balanced with label restrictions such as re-entry intervalsand preharvest intervals. Application and product costs have been calculated to develop cost-effective control programs to reducethe number of SLF insecticide applications from the current 14 back toward a pre-SLF average of only four. About 15insecticides have been evaluated for efficacy on SLF overwintering eggs, with only the organophosphate, chlorpyrifos, being effective. Although SLF has been found feeding on apple and peach late season, it does not appear to be a significant tree fruit pest yet. On-line extension control recommendations for SLF on grape, tree fruit and ornamentals are available to the public and are updated regularly.After an initial trial with a formulation of the organic product,Beauveria bassiana, proved successful in large plot trials in a Norristown, PA park in 2019, a muchlarger scale and intensive, replicated trial including seven treatments appliedboth by helicopterand by ground equipment ata state park in 2020. Despite Covid 19 restrictions on travel and summer help, it is being evaluated for efficacy, residual activity, cost, and non-target impacts on pollinators and other arthropod bioindicator taxa. Based on preliminary evaluations, the neonicotinoid (dinotefuron) was very effective both by ground and by air for at least three weeks and appears to have had a minimal impact on bees and other non-target aerial and ground arthropods probably due to the systemic nature of the product which allows it to be quickly absorbed through the foliage into the SLF foodplants, and minimizes residues to non-targets not feeding on the plant within oneto twodays. Unfortunately, the two Beauveria formulations which were applied three times compared to the dinotefuron being applied only once, was less effective in controlling SLF than seen in the 2019 Norristown trial. Impacts on non-target arthropods also appear to have been minimal though.

Publications

• Type: Websites Status: Published Year Published: 2020 Citation: Spotted Lanternfly Management for Residents. H. Leach, D. Biddinger, G. Krawczyk, & A. Korman. 2020. https://extension.psu.edu/spotted-lanternfly-management-for-residents
• Type: Other Status: Published Year Published: 2020 Citation: The spread of spotted lanternfly. Matt Milkovich & D. Biddinger. March 19,2020. Good Fruit Grower. https://www.goodfruit.com/the-spread-of-spotted-lanternfly/
• Type: Books Status: Published Year Published: 2020 Citation: Managing Eastern Apple orchards for Pollinators and Other Beneficial Insects. Hopwood, J., E. Rajotte, K. Gill, M. Vaughan, E. Lee-Mader, E. May, A. Code, N. Joshi, and D. Biddinger. 86 p. 2020. D. Biddinger, https://extension.psu.edu/managing-eastern-apple-orchards-for-pollinators-and-other-beneficial-insects-production
• Type: Websites Status: Published Year Published: 2020 Citation: Spotted Lanternfly Management in Vineyards. August 20, 2020 H. Leach, D. biddinger, G. Krawczyk, & M.Centinari. https://extension.psu.edu/spotted-lanternfly-management-in-vineyards.
• Type: Journal Articles Status: Published Year Published: 2019 Citation: Acebes-Doria, A, A. Agnello, D. Alston, H. Andrews, E. Beers, C. J. Bergh, R. Bessin, B. Blaauw, D.G. Buntin, E. Burkness, S. Chen, T. Cottrell, K. Daane, L. Fann, S. Fleisher, C. Guedot, L. Gut, G. Hamilton, R. Hilton, K. Hoelmer, W. Hutchison, P. Jentsch, G. Krawczyk, T. Kuhar, J. Lee, J. Milnes, A. Nielsen, D. Patel, B. Short, A. Sial, L. Spears, K. Tatman, M. Toews, J. Walgenbach, C. Welty, N. Wiman, J. van Zoeren, and T. Leskey. 2019. Season-long Monitoring of the Brown Marmorated Stink Bug, Halyomorpha halys (St�l) (Hemiptera: Pentatomidae), Throughout the United States using Commercially Available Traps and Lures. J. Econ. Entomol. doi: 10.1093/jee/toz240
• Type: Other Status: Published Year Published: 2019 Citation: Krawczyk, G., H. Morrin and C. Hirt. 2019. Alternative methods to manage brown marmorated stink bug, Halyomorpha halys. IOBC-WPRS Bulletin 146 (2019):114-118
• Type: Other Status: Published Year Published: 2019 Citation: Peterson, H., J. Ali and G. Krawczyk. 2019. Biocontrol of invasive Halyomorpha halys. IOBC-WPRS Bulletin 146 (2019): 119-120
• Type: Other Status: Published Year Published: 2019 Citation: Krawczyk, G., H. Leach, C. Hirt, H. Rice and J. Urban. 2019. Potential New Invasive Pest Species in United States  Spotted Lanternfly, Lycorma delicatula. IOBC-WPRS Bulletin 146 (2019): 132-136.
• Type: Websites Status: Published Year Published: 2020 Citation: L�pez-Uribe MM, Underwood RM. (2020). How to Keep Bees During COVID-19. Pennsylvania State Extension (Newsletter Article) https://extension.psu.edu/orchard-pollination-strategies-for-maintaining-pollination-services-in-tree-fruit. Also available in Spanish.
• Type: Websites Status: Published Year Published: 2019 Citation: Grozinger CM, Underwood RM, L�pez-Uribe MM (2019). Viruses in Honey Bees. Pennsylvania State Extension (Factsheet). https://extension.psu.edu/viruses-in-honey-bees
• Type: Websites Status: Published Year Published: 2019 Citation: L�pez-Uribe MM (2019). Beneficial Insects and Pollinators. Chapter in: IPM for Pennsylvania Schools and Childcares, A How to Manual. Pennsylvania State Extension (Factsheet) https://extension.psu.edu/ipm-for-pennsylvania-schools-and-childcares-a-how-to-manual
• Type: Websites Status: Published Year Published: 2019 Citation: L�pez-Uribe MM, Underwood RM. (2019). Honey Bee Diseases: American Foulbrood. Pennsylvania State Extension (Factsheet) https://extension.psu.edu/honey-bee-diseases-american-foulbrood
• Type: Websites Status: Published Year Published: 2019 Citation: Underwood RM, L�pez-Uribe MM. (2019). Methods to Control Varroa Mites: An Integrated Pest Management Approach. Pennsylvania State Extension https://extension.psu.edu/methods-to-control-varroa-mites-an-integrated-pest-management-approach
• Type: Journal Articles Status: Awaiting Publication Year Published: 2020 Citation: Sponsler, D.B., Shump, D., Richardson, R., Grozinger, C.M. Characterizing the floral resources of a North American metropolis using a honey bee foraging assay Ecological Applications (in press).
• Type: Journal Articles Status: Awaiting Publication Year Published: 2020 Citation: C.M. Grozinger and A. Zayed. Genomics for understanding and improving pollinator health in a world of multiple stressors Nature Reviews Genetics (in press).
• Type: Journal Articles Status: Published Year Published: 2020 Citation: Douglas, M.R., Sponsler, D.B., Lonsdorf, E.V. and C.M. Grozinger. County-level analysis reveals a rapidly shifting landscape of insecticide hazard to honey bees (Apis mellifera) on US farmland Scientific Reports 10(1), 1-11.
• Type: Journal Articles Status: Published Year Published: 2019 Citation: Erickson, E., Adam. S., Russo, L., Wojcik, V., Patch, H.M., and C.M. Grozinger. More than meets the eye: The role of ornamental plants in supporting pollinators Environmental Entomology doi: 10.1093/ee/nvz133 (2019).
• Type: Journal Articles Status: Published Year Published: 2019 Citation: Sponsler, D.B., Grozinger, C.M., Hitaj, C., Rundl�f, M., Bot�as, C, Code, A., Lonsdorf, E.V., Melathopoulos, A.P., Smith, D.J., Suryanarayanan, S., Thogmartin, W.E., Williams, N.M., Zhang, M., and M. R. Douglas. Pesticides and pollinators: a socioecological synthesis. Science of the Total Environment 662: 1012-1027 (2019).
• Type: Journal Articles Status: Published Year Published: 2019 Citation: lenniken, M.L. and C.M. Grozinger. Bee Viruses: Ecology, Pathogenicity, and Impacts. Annual Review of Entomology 64: 205-226 (2019).

Progress 10/01/18 to 09/30/19

Outputs
Target Audience:Target audiences include the 450 fruit growers in Pennsylvania and equivalent numbers in the adjacent mid-Atlantic fruitgrowing regions of Delaware, Maryland, Virginia, West Virginia, New York, New Jersey,and North Carolina. Many presentations have been made at professional meetings to peer scientists, government officials, pesticide industry, and policy makers in various agencies within USDA, including APHIS, NRCS, ARS, and NIFA as well as EPA. The public has been engaged through large field days at the PSU Research Station, through workshops with the Xerces Society and PASA (PA Sustainable Agric.) and several on-line publication through the NE IPM centers, Penn State Center for Pollination Research, USDA-NRCS publications, and the Xerces Society website. Most audiences are aware of problems with pollinators, especially the honey bee, but are not aware of alternative pollinators, how to conserve pollinators with appropriate habitat, and especially the role of pesticides in this decline. We have also reached an international audience of researchers through an international pollinator conference at Penn State, Entomological Societey of America national and international meetings, and collaborations with researchers in Columbia and Europe with pollinatorsand multiple trips to work on BMSB in Georgia and Europe where our research and publications on the adaptation of native biological control agents of Pentatomidae to the invasive BMSB and control tactics are helping them deal with it. Fruit growers and homeowners will recieve updated reccomendations on pesticide impacts and conservation of both honey bees and native bees as well a biological control agents of pests in the revised 2018- 19 edition of the Penn State Tree Fruit Production Guide. This guide has always been available on-line and is considered on of the most complete and effective guides of its type in the US and internationally recognized. The concept of integrating pollinator protection into IPM was proposed in a publication by Biddinger & Rajotte and has now been accepted by the Entomological Society of American's Pollinator Health Position Statement and in several USDA grant programs including SCRI and AFRI and so have reached a much larger audience than just tree fruit growers. Publication with the Xerces Society have reached far beyond the 2% of the population that are farmers, but are now influencing the general public with over 100,000 downloads on the How Neonicotinoid Insecticides Can Kill Bees review series and technical manuals with USDA-NRCS on pollinator wildflower plantings and perennial hedgerows are informing many other agricultural crops and regions than the just the mid-Atlantic states. The IPPM concept is taught in IPM graduate courses at Penn State by Rajotte and Biddinger and in winter extension presentations to fruit growers and Master Gardeners. Changes/Problems:Spotted Lanternfly has become such a significant economic pest on grape and political quarantine problem that the focus, time and resourcesof Biddinger and Krawczyk has been increasingly taken away from normal fruit IPM to developing control tactics for this pest rather at the expense of further developing IPM programs and tactics for controlling tree fruit pests and conserving beneficial arthroopods and pollinators. With the early retirement of the PSU grape entomologist, I my tree fruit research responsibilities have temporarily been expanded to include grapes for the SLF emergency. SLFis very difficult to maintain in colonies within the quarantine facilities. Small potted trees or vines do not seem to provide enough sap for long-term development of adults or nymphs, but rearing has improved by frequent substitution of new tree of heaven and grape vines. Conducting SLF research within the quarantine zone is difficult as it is 3 hours from the PSU campus and 2 hours from the Fruit Research and Extenson Center in Biglerville. Getting 50% of a technician's time at the PSU Berks campus and the hiring of an extension associate to work on SLF within the quarentine has greatly increased productivity and reduced road travel time. As pesticide companies continue to consolidate through mergers and experience financial difficulties, grant in-aid for pesticide testing is becoming more unpredictable and it is becoming more difficult to maintain research orchards and personnel for this type of research. What opportunities for training and professional development has the project provided?A total of 23 undergraduates, 9 graduate students, and one post-doctoral scholar were trained in various aspects of pollinator ecology and toxicology, invasive species biology and control, and IPPM in tree fruit and grape. How have the results been disseminated to communities of interest?Over 40 extension presentations have been made to fruit growers, bee keepers, and the interested public. Several fact sheets on various aspects of SLF biology and control are available to the public at the PSU extension website. Dozens of interviews to trade journals, newspapers, and government agencies have been made on-going SLF research and control efforts for tree fruit pests and conserving biological control of secondary pests. Several dozen peer-reviewed publications have informed the scientific community, as well as departmental seminars and presentations at professional societies. What do you plan to do during the next reporting period to accomplish the goals?Collaborators will 1) perform research on Spotted Lanternfly (SLF) addressing questions bridging a range of applied to basic aspects of SLF biology, and 2) integrate results from research findings into a strategic management plan of SLF that provides short-term immediate solutions to the current danger of SLF in Pennsylvania, and sustainable long-term solutions to mitigate SLF spread and damage to other locations within the US. We will continue to evaluate new and registered insecticides for tree fruit pests, develop bettter methods for monitoring and timing of insecticide interventions while trying to conserve pollinators and biological control agents of secondary pests such as mites, scale, and aphids.

Impacts
What was accomplished under these goals? Objective 1 (Biddinger & Krawczyk). Concerns about insecticide resistance in the main apple pest, codling moth, due to some control failures in FREC trials over the last couple of years, have prompted increased testing of alternative products to Delegate (spinetoram) as rotation partners to the diamide Altacor (renaxypyr) and the initiation of laboratory bioassays to quantify resistance levels and frequency. We continue to evaluate in our experimental orchards on station any new insecticides being developed by various agrichemical companies, but mergers of several of these companies have put a hold on development of new products with only Enkounter (acetamiprid + methoxyfenozide pre-mix) being the only product being registered in the 2020 season. We have established that it is a good resistance management rotation partner with the existing codling moth insecticides with differing modes of action. Additionally, baseline trials of laboratory and field colonies of codling moth have begun at the FREC labs to determine levels of resistance to the diamide insecticides and spinetoram which are the keystone control methods for this key pest of apple. Objectives 1 and 3 (Krawczyk). Evaluations of long-lasting insecticide treated nets to manage brown marmorated stink bug (BMSB) and spotted lanternfly (SLF) in fruit systems. Although the research is still ongoing, the initial results are very promising. By deploying nets baited with BMSB attractant around orchards, growers should be able to reduce or even eliminate insecticide applications targeting this pest. The same net as deployed against BMSB, is also effective in killing SLF, however the lack of effective SLF attractant makes this method less useful for this pest. The activities under the USAID REAP Program in the Republic of Georgia resulted in the development of national BMSB management program in this country, which is generally based on the alternative management of BMSB. Objectives 1 and 4 (Biddinger). San Jose scale is becoming more problematic for PA fruit growers due to resistance to chlorpyrifos and growers discontinuing the use of dormant oil because of cost, incompatibility with fungicides like Captan, and because it no longer is needed for mite control due to the successful implementation of biological mite control from the phytoseiid predatory mite, Typhlodromus pyri. Control measures for SJS are now shifting more to controlling the immature SJS crawlers post-bloom rather than trying to suffocate overwintering adults with oil. To this end we are trapping SJS adult males with special pheromone traps to further refine a degree day model for precise timing of sprays for the short window that the susceptible crawlers are vulnerable. The SJS pheromone lure is also very attractive to the main biological control wasp, Encarsia perniciosus, which are also monitoring to determine periods of vulnerability to pesticides that should be avoided to conserve them and to determine if a parasitoid/prey ratio can be used as a spray threshold, since one does not exist other than fruit damage from the previous season. At least a dozen insecticides have been evaluated for SJS control pre- and post-bloom and if they will give summer aphid control at SJS timings. Objectives 1 and 5 (Biddinger, Krawczyk, Lopez-Uribe). We continue to test pesticides on tree fruit pests, but additionally have be determining field realistic doses in nectar and pollen when they are applied pre-bloom to petal fall and are finding some fungicides to be much more toxic to bees than previously thought. In trials comparing honey bee susceptibility to Osmia bees, we have found Osmia to generally be much more susceptible to both insecticides and fungicides than the honey bee. This work is being conducted by two Ph.D. students and much of it will be published in the next 6 months. A M.S. student started this summer to evaluate the effect of SLF insecticide sprays in forestry and fruit crops to pollinators, beneficial insects and other non-targets. Long-term bee monitoring studies to look for pollinator declines since 2009 continue with approximately 120,000 bees and 15, 000 syrphid flies having been collected to date representing over 250 bee species and 40 syrphid species found in apple and cherry orchards. We have changed apple pre-bloom insecticide recommendations for neonicotinoid applications from pink to about 2 weeks earlier at 1/2 inch green stage for the OP and carbamate resistant pest, rosy apple aphid, to reduce insecticide levels found in the nectar and pollen and only recommend two of the safest neonicotinoid insecticides out of the 7 recommended. We have evaluated and now recommend Beleaf (flonicamid) as a bee-safe alternative for RAA control pre-bloom as late as the pink stage. Additionally, we are evaluating the effects of common pre-bloom and bloom fungicides on both the honey bee and Osmia and found some products to be much more toxic to Osmia. Objective 2 (Biddinger & Krawczyk). Mating Disruption research has been reduced as invasive pests such as Spotted Lanternfly, Spotted Wing Drosophila, and Brown Marmorated Stink Bug have resulted the need for more traditional contact and systemic insecticides than before, leaving expensive, target specific pheromone mating disruption at a major disadvantage in cost, so that the use of mating disruption in orchards has declined. Pheromone research is now concentrating on finding compounds attractive to BMSB and SLF that can be used for monitoring populations, but none of the products have proven to be effective enough for large scale mating disruption, especially since both of these pests mostly mate outside of orchard in the local landscape and then move into orchards already mated. Objective 3 (Biddinger & Rajotte). Evaluations of the bioinsecticides, Beauveria bassiana and Isaria sp are being evaluated for control in agricultural crops, ornamental nurseries, and forests. SLF control has been better in both large scale plots and on potted trees and vines than originally thought and different formulations and application methods are being examined to improve efficacy and residual, include a ultra-low volume, oil-based formulation for aerial applications. Objectives 3 and 4 (Biddinger & Krawczyk). The new invasive pest spotted lanternfly (SLF) - Approximate 50 insecticides have been evaluated for contact and residual activity on Spotted Lanternfly adults and nymphs at both grape and peach label rates. From these trials, 15 insecticides have had 2e label amendments to add SLF to the list of pests that each compound will control. Without this, applications for SLF would be off label and would be "targeting other late season pests", so that product failures would not be covered by the manufacturer. Many products were found to be effective on SLF, but long residual activity reduce the number of applications has to be balance with label restrictions such as re-entry intervals (REI) and preharvest intervals (PHI). Application and product costs have been calculated to develop cost-effective control programs to reduce the number of SLF insecticide applications from the current 14 back toward a pre-SLF average of only 4. About 10 insecticides have been evaluated for efficacy on SLF overwintering eggs, with only the organophosphate, chlorpyrifos being effective. Although SLF has been found feeding on apple and peach late season, it does not appear to be a significant tree fruit pest yet. On-line extension control recommendations for SLF on grape, tree fruit and ornamentals are available to the public and are undated regularly.

Publications

• Type: Journal Articles Status: Published Year Published: 2018 Citation: Zaleski, A. America isnt ready for the lanternfly invasion. Bloomberg Businessweek. Oct. 2, 2018. https://www.bloomberg.com/news/features/2018-10-02/america-isn-t-ready-for-the-lanternfly-invasion
• Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Heller, S., Joshi, N. K., Leslie, T., Rajotte, E., and D. Biddinger. 2019. Diversified floral resource plantings support bee communities after apple bloom in commercial orchards. Nature Scientific Reports. (accepted Sept. 2019).
• Type: Journal Articles Status: Submitted Year Published: 2019 Citation: Joshi N.K., and D. J. Biddinger. Nest manipulation protects developmental stages of the Japanese orchard bee (Osmia cornifrons) from a cleptoparasitic mite pest. Journal of Applied Entomology. (In Review)
• Type: Journal Articles Status: Published Year Published: 2019 Citation: Leach, H., D. Biddinger, G. Krawczyk, E. Smyers, J. M. Urban. 2019. Evaluation of insecticides for control of the spotted lanternfly, Lycorma delicatula, (Hemiptera: Fulgoridae), a new pest of fruit in the northeastern U.S. Crop Protection 124(2019) 104833.
• Type: Book Chapters Status: Published Year Published: 2018 Citation: Biddinger, D., E. G. Rajotte, N. K. Joshi*. 2018. Chapter. 4 Integrating pollinator health into tree fruit IPM- A case study of Pennsylvania apple production (Chapter- 4), p. 69-83. In: The pollination of cultivated plants: a compendium for practitioners. Vol. 1. (Editor- D. Roubik). Food and Agricultural Organization of the United Nations. 313 p. https://ainfo.cnptia.embrapa.br/digital/bitstream/item/180143/1/I9201EN-1.pdf
• Type: Book Chapters Status: Published Year Published: 2018 Citation: Biddinger, D. 2018. Conserving predatory mites in apple orchards (or mighty mites conquer mite pests). Box 5.1, pg. 88-89. In: Natural Enemies: An Introduction to Biological Control. 2nd edition. A. Hajek & J. Eilenberg. Cambridge University Press. 439 p.
• Type: Conference Papers and Presentations Status: Published Year Published: 2018 Citation: Leslie, T. W., N. K. Joshi, G. Krawczyk, & D. Biddinger. 2018. Parasitism of the invasive brown marmorated stink bug by a native tachinid fly (Poster 86). 9th International IPM Symposium, March 19-22, 2018. Baltimore, MD. https://ipmsymposium.org/2018/Documents/IPMSymp18_Full_Program_with_Abstracts.pdf
• Type: Conference Papers and Presentations Status: Published Year Published: 2018 Citation: Joshi, N. K., T. W. Leslie, E. G. Rajotte, & D. J. Biddinger. 2018. Integrated pest and pollinator management: Investigating impacts of different pesticide programs on pollinator communities in commercial orchards (Poster 103). 9th International IPM Symposium, March 19-22, 2018. Baltimore, MD. https://ipmsymposium.org/2018/Documents/IPMSymp18_Full_Program_with_Abstracts.pdf
• Type: Conference Papers and Presentations Status: Published Year Published: 2018 Citation: Understanding and Mitigating the Risks of Pesticide Exposure for Pollinators and Other Beneficial Insects. 2018 Entomological Society of America Annual Meeting, Nov. 11-14, 2018. Vancouver, BC, Canada. Organizer: Nigel Raine, Univ. of Guelph, Ontario, Canada Invited Speaker: D. Biddinger, E. Rajotte, N. Phan**, & N. Joshi*. Minimizing pesticide impacts on wild pollinators in eastern apple orchards through integrated pest and pollinator tactics.
• Type: Conference Papers and Presentations Status: Published Year Published: 2018 Citation: Integrate Pest and Pollinator Management (IPPM): Integrating Pollinator Protection into Fruit and Nut IPM Programs. 9th International IPM Symposium, March 19-22, 2018. Baltimore, MD. Symposium #10. Organizers: D. Biddinger & N. Joshi. https://ipmsymposium.org/2018/Documents/IPMSymp18_Full_Program_with_Abstracts.pdf Invited Speaker: Joshi, N., M. Park, B. Danforth, D. Biddinger, & E. Rajotte. 2018. Apple grower pollination practices and perceptions of alternative pollinators in New York and Pennsylvania.
• Type: Conference Papers and Presentations Status: Published Year Published: 2018 Citation: Integrate Pest and Pollinator Management (IPPM): Integrating Pollinator Protection into Fruit and Nut IPM Programs. 9th International IPM Symposium, March 19-22, 2018. Baltimore, MD. Symposium #10. Organizers: D. Biddinger & N. Joshi. https://ipmsymposium.org/2018/Documents/IPMSymp18_Full_Program_with_Abstracts.pdf.Invited Speaker: Biddinger, D., E. Rajottte, & N. Joshi. 2018. Integrated pest and pollinator management in Pennsylvania apple orchards.
• Type: Journal Articles Status: Published Year Published: 2019 Citation: L�pez-Uribe MM, Jha S, Soro A. (In press) A trait-based approach to predict population genetic structure in bees. Molecular Ecology doi.org/10.1111/mec.15028
• Type: Journal Articles Status: Published Year Published: 2019 Citation: Underwood RM, Traver BE, L�pez-Uribe MM (2019) Beekeeping management practices are associated with operation size and beekeepers philosophy towards in-hive chemicals. Insects 10: 10 doi.org/10.3390/insects10010010
• Type: Journal Articles Status: Published Year Published: 2018 Citation: Ryan SF, Adamson NL, Aktipis A, Andersen LK, Austin R, Barnes L, Beasley MR, Bedell KD, Bidell K, Briggs S, Chapman B, Cooper C, Corn J, Creamer NG, Delborne JA, Domenico P, Driscoll E, Goodwin J, Hjarding A, Hulbert JM, Isard S, Just MG, Kar Gupta K, L�pez-Uribe MM, OSullivan J, Landin J, Landis EA, McKenney EA, Madden AA, LM Nichols LM, Ramaswamy S, Reading B, Russell S, Sengupta N, Shell L, Sheard JK, Shoemaker DD, Sorger DM, Starling C, Thakur S, Vatsavai R, Weinstein M, P Wimfrey, Dunn RR (2018) The Role of Citizen Science in Addressing Grand Challenges in Food and Agriculture Research. Proceedings of the Royal Society of London B 285 (1891), 20181977 doi.org/10.1098/rspb.2018.1977
• Type: Journal Articles Status: Published Year Published: 2018 Citation: Vaudo AD, Fritz ML, L�pez-Uribe MM. (2018) Opening the door to the past: what new genetic information can be accessed from museum curated bees. Insects Systematics and Diversity 2 (5), 4 doi.org/10.1093/isd/ixy014
• Type: Journal Articles Status: Published Year Published: 2018 Citation: Grando C, Amon ND, Clough S, Guo N, Wei W, Azevedo P, L�pez-Uribe MM, Zucchi MI (2018) Two Colors, One Species: The case of Melissodes nigroaenea (Apidae: Eucerini), an important pollinator of cotton fields in Brazil. Sociobiology 65 (4), 645-653 doi: 10.13102/sociobiology.v65i4.3464
• Type: Journal Articles Status: Published Year Published: 2018 Citation: Penick CA, Halawani O, Pearson B, L�pez-Uribe MM, Mathews S, Dunn RR, Smith AA. (2018) External immunity in ant societies: Sociality and colony size do not predict investment in antimicrobials. Royal Society Open Science 5(2): 171332. doi: 10.1098/rsos.171332
• Type: Journal Articles Status: Published Year Published: 2018 Citation: Dorchin A, L�pez-Uribe MM, Praz CJ, Griswold T, Danforth BN (2018) Phylogeny and new generic-level classification of the Eucera complex (Hymenoptera: Apidae: Eucerini partim). Molecular Phylogenetics and Evolution 119:81-92. doi: 10.1016/j.ympev.2017.10.007
• Type: Other Status: Published Year Published: 2018 Citation: Book Review: L�pez-Uribe MM (2018) Pollination services to agriculture: Sustaining and enhancing a key ecosystem service. American Entomologist 64 (1): E1 doi.org/10.1093/ae/tmx070
• Type: Conference Papers and Presentations Status: Other Year Published: 2018 Citation: L�pez-Uribe MM. Bees, domestication and agriculture: An evolutionary story (Keynote speaker). Bee Conservation Meeting at York University. Toronto, Canada. (November 2018)
• Type: Conference Papers and Presentations Status: Other Year Published: 2018 Citation: L�pez-Uribe MM, Simone-Finstrom M. Pollinator Health: Integrating ecological, genetic and physiological factors (Invited talk). Entomological Society of America Meeting (ESA), SEC and ESCB Joint Annual Meeting. Vancouver, BC, Canada (November 2018)
• Type: Conference Papers and Presentations Status: Other Year Published: 2018 Citation: L�pez-Uribe MM. Bee conservation genetics: molecular tools for the study of pollinator populations in changing environments (Keynote speaker). XII Encontro sobre Abelhas. Uberlandia, Brazil (October 2018)
• Type: Conference Papers and Presentations Status: Other Year Published: 2018 Citation: Kilpatrick SK, L�pez-Uribe MM, Hines HM. The role of cucurbit domestication on the evolutionary history of squash bees [Hymenoptera: Apidae: Eucera (Peponapis) and (Xenoglossa)] (Oral presentation) Entomological Society of America, Vancouver, BC, Canada (November 2018)
• Type: Conference Papers and Presentations Status: Other Year Published: 2018 Citation: Slone JD, Burrack H, L�pez-Uribe MM. Integrating pest and pollinator management (Symposium presentation) Entomological Society of America Annual Meeting, Vancouver Canada (November 2018)
• Type: Conference Papers and Presentations Status: Other Year Published: 2018 Citation: Hinshaw CH, Evans KC, Grozinger CM, L�pez-Uribe MM. Tracking Feral Bee Health in Pennsylvania (Invited Speaker) Entomological Society of America Annual Meeting, Vancouver, BC, Canada (November 2018)
• Type: Conference Papers and Presentations Status: Other Year Published: 2018 Citation: Kilpatrick SK, Gibbs J, Mikulas MM, Spichiger S, Ostiguy N, Biddinger D, Lopez-Uribe MM. An updated checklist of the bees (Hymenoptera: Apoidea: Anthophila) of Pennsylvania, United States of America. Pennsylvania Beekeeping Association Meeting, State College PA (November 2018)
• Type: Conference Papers and Presentations Status: Other Year Published: 2018 Citation: Lawrence BL, Madden AA, Dunn RR, Underwood RM, L�pez-Uribe MM. The Honey Bee Colony Microbiome: Miticides, Geography, or Both? (Poster presentation) Pennsylvania Beekeeping Association Meeting, State College PA (November 2018)
• Type: Conference Papers and Presentations Status: Other Year Published: 2018 Citation: Hinshaw CH, Evans KC, Grozinger CM, L�pez-Uribe MM. Tracking Feral Bee Health in Pennsylvania (Poster presentation) Pennsylvania State Beekeepers Association Conference, State College, PA (November, 2018)
• Type: Conference Papers and Presentations Status: Other Year Published: 2018 Citation: Evans KC, L�pez-Uribe MM. Efficacy of Oxalic Acid (OA) applications and requeening in reducing varroa mite infestations in honey bee packages (Poster presentation) Pennsylvania State Beekeepers Association, State College PA (November 2018)
• Type: Other Status: Awaiting Publication Year Published: 2019 Citation: Niedermeier, M., D. Lerman, B. Dodson, M. Lopez-Uribe, E. Machtinger, M. Skvarla and E. Rajotte. 2019. IPM for Pennsylvania Schools: A how-to manual. In press. 3rd edition. 183 pages
• Type: Journal Articles Status: Published Year Published: 2019 Citation: Maria Mazin, Stefanos S. Andreadis, Nina E. Jenkins, Kevin R. Cloonan, T.C. Baker, Ed G. Rajotte: Activity and distribution of the mushroom phorid fly, Megaselia halterata , in and around commercial mushroom farms. Entomologia Experimentalis et Applicata 04/2019;, DOI:10.1111/eea.12777
• Type: Journal Articles Status: Published Year Published: 2019 Citation: Joseph Walls, Edwin Rajotte, Cristina Rosa: The Past, Present, and Future of Barley Yellow Dwarf Management. 01/2019; 9(1):23., DOI:10.3390/agriculture9010023
• Type: Journal Articles Status: Published Year Published: 2018 Citation: Mitzy Porras, Consuelo M. De Moraes, Mark C. Mescher, Edwin G. Rajotte, Tom�s A. Carlo: A plant virus (BYDV) promotes trophic facilitation in aphids on wheat. Scientific Reports 12/2018; 8(1)., DOI:10.1038/s41598-018-30023-6
• Type: Journal Articles Status: Published Year Published: 2018 Citation: S Paudel, I Mik�, A Deans, E Rajotte, G Felton. 2018. Lyonets gland of the tomato fruitworm, Helicoverpa zea (Lepidoptera: Noctuidae). PeerJ Preprints 6, e26455v1
• Type: Conference Papers and Presentations Status: Other Year Published: 2019 Citation: Leach, H., D. Biddinger, & J. Urban. Management of spotted lanternfly in fruit crops. Eastern Branch Entomological Society of America 90th Annual Meeting, March 9-12, 2019. Blacksburg, Virginia.
• Type: Journal Articles Status: Published Year Published: 2018 Citation: A Singh, LP Sah, Y Dhoj GC, M Devkota, LA Colavito, BP Rajbhandari, G Norton, EG Rajotte, R Muniappan. 2018. Evaluation of pest exclusion net to major insect pest of tomato in Kavre and Lalitpur. Nepalese Journal of Agricultural Sciences 16, 128-137
• Type: Conference Papers and Presentations Status: Other Year Published: 2019 Citation: Challenges of Integrated Pest Management (IPM) in High Value Commodities. Eastern Branch Entomological Society of America 90th Annual Meeting, March 9-12, 2019. Blacksburg, Virginia. Organizers: A. Leach & H. Leach. Invited Speaker: D. Biddinger, E. Rajotte, N. Joshi, & H. Leach. A 30 year perspective by entomologists on how IPM programs have changed and been challenged in eastern tree fruits.
• Type: Conference Papers and Presentations Status: Other Year Published: 2018 Citation: Understanding and Mitigating the Risks of Pesticide Exposure for Pollinators and Other Beneficial Insects. Entomological Society of America Annual Meeting, Nov. 11-14, 2018. Vancouver, BC, Canada. Organizer: Nigel Raine, Univ. of Guelph, Ontario, Canada Invited Speaker: D. Biddinger, E. Rajotte, N. Phan**, & N. Joshi*. Minimizing pesticide impacts on wild pollinators in eastern apple orchards through integrated pest and pollinator tactics.
• Type: Conference Papers and Presentations Status: Other Year Published: 2019 Citation: Kilpatrick, S., J. Gibbs, M. Mikulas, S.-V. Spichiger, N. Ostiguy, D. Biddinger, & M. Lopes-Uribe. An updated checklist of the bees (Hymenoptera: Apoideas: Anthophila) of Pennsylvania. Eastern Branch Entomological Society of America 90th Annual Meeting, March 9-12, 2019. Blacksburg, Virginia.
• Type: Conference Papers and Presentations Status: Other Year Published: 2019 Citation: Leach, H.*, M. Centinari, D. Biddinger, & J. Urban. Spotted lanternfly damage and phenology in Pennsylvania vineyards. 94th Cumberland-Shenandoah Fruit Workers Conference. Winchester, VA, Nov 29-30, 2018.
• Type: Conference Papers and Presentations Status: Other Year Published: 2018 Citation: Biddinger, D.*, H. Leach, & J. Urban. Residual control of spotted lanternfly nymphs and adults with various insecticides. 94th Cumberland-Shenandoah Fruit Workers Conference. Winchester, VA, Nov 29-30, 2018.
• Type: Conference Papers and Presentations Status: Other Year Published: 2018 Citation: Joshi, N.*, E. Rajotte, K. Nathani, & D. J. Biddinger. Foraging and dispersal behavior of Osmia cornifrons in an apple orchard ecosystem. 2018 Entomological Society of America Annual Meeting, Nov. 11-14, 2018. Vancouver, BC, Canada
• Type: Conference Papers and Presentations Status: Other Year Published: 2018 Citation: Crone, M.*, N. Phan, D. Biddinger, & C. Grozinger. The effects of diet on honey bee (Apis mellifera) pesticide sensitivity. 2018 Entomological Society of America Annual Meeting, Nov. 11-14, 2018. Vancouver, BC, Canada
• Type: Conference Papers and Presentations Status: Other Year Published: 2018 Citation: Phan, N.*, E. Rajotte, & D. Biddinger. Sublethal pesticide exposure increases developmental time and reduces rate of weight gain in Osmia cornifrons larvae. (Virtual Poster). 2018 Entomological Society of America Annual Meeting, Nov. 11-14, 2018. Vancouver, BC, Canada
• Type: Conference Papers and Presentations Status: Other Year Published: 2018 Citation: Kilpatrick, S.*, J. Gibbs, M. Mikulas, S. Spichiger, N. Ostiguy, D. Biddinger, M. Lopez-Uribe. An updated checklist of the bees (Hymenoptera: Apoidea: Anthophila) of Pennsylvania, United States. (poster). 2018 Entomological Society of America Annual Meeting, Nov. 11-14, 2018. Vancouver, BC, Canada
• Type: Conference Papers and Presentations Status: Other Year Published: 2018 Citation: Leach, H.*, M. Centinari, D. Biddinger, & J. Urban. Response and management of the invasive, spotted lanternfly, in grape. 2018 Entomological Society of America Annual Meeting, Nov. 11-14, 2018. Vancouver, BC, Canada
• Type: Conference Papers and Presentations Status: Other Year Published: 2018 Citation: Pak, D.*, D. J. Biddinger, & O. Bj�rnstad. 2018. The role of diapause in the developmental synchrony of an agricultural pest: a case study with the tortricid pest Cydia pomonella. Presented at the Ecological Society of America, New Orleans, LA (2018).
• Type: Journal Articles Status: Published Year Published: 2018 Citation: Murvanidze, M., G. Krawczyk, N. Inasaridze, L. Dekonoidze, N. Samsonadze, M. Macharasvilli, S. Khutsishvilli and S. Shengelaia. 2018. Preliminary data on the biology of brown marmorated stink bug Halyomorpha halys (Hemiptera, Pentatomidae) in Georgia. Turk J. Zool. 42:617-624; doi:10.3906/zoo-1802-34
• Type: Journal Articles Status: Published Year Published: 2018 Citation: Krawczyk, G., H. Morin and C. Hirt. 2018. Alternative methods to manage brown pest management marmorated stink bug Halyomorpha halys (Stal) as component of IPM practices in Pennsylvania orchards. Pennsylvania Fruit News 98(1): 17-19
• Type: Book Chapters Status: Published Year Published: 2018 Citation: Ioriatti, C., G. Angeli and G. Krawczyk. 2018 Optimizing insecticide use in integrated management of fruit insect pests. Chapter in Management of fruit pests ed. By M. Fountain. http://dx.doi.org/10.19103/AS.2019.0046.28 (Burleigh Dodds Science Publishing Limited)
• Type: Conference Papers and Presentations Status: Other Year Published: 2018 Citation: Krawczyk, G. 2018. Brown marmorated stink bug management options. Conference on Fighting Against Halyomorpha halys  Experiences, Results and Prospects. Republic of Georgia National Food Agency and Ferrero Company Conference, Tbilisi, Georgia. Dec 2018
• Type: Conference Papers and Presentations Status: Other Year Published: 2018 Citation: Krawczyk, G., H. Peterson and C. Hirt. 2018. BMSB and SLF  field trials during the 2018 season. 94th Cumberland-Shenandoah Fruit Workers Conference. Winchester, VA. Nov 2018
• Type: Conference Papers and Presentations Status: Other Year Published: 2018 Citation: Peterson, H. M., Hirt, C., Krawczyk, G. Comparing parasitism of brown marmorated stink bug (Halyomorpha halys (St�l)) sentinel egg masses in Pennsylvania fruit orchard landscapes. 94th Cumberland-Shenandoah Fruit Workers Conference. Winchester, VA. Nov 2018.
• Type: Conference Papers and Presentations Status: Other Year Published: 2018 Citation: Peterson, H. M., Hirt, C., Krawczyk, G. An Update on the presence of the samurai wasp, Trissolcus japonicus, in Pennsylvania. Brown Marmorated Stink Bug Areawide Project and IPM Working Group Meeting. Winchester, VA. Nov 2018
• Type: Conference Papers and Presentations Status: Other Year Published: 2018 Citation: Anderson, T., M. Bufington, G. Krawczyk, N. Larson, W. Morrison, S. Simon and M. Wright. 2018. Invasive Species Security: Protecting Our National Health, Food Supply and Environment. A Science Policy Field Tour. A special presentation and poster, Entomological Society of America Annual Meeting. Vancouver, B.C. Nov 2018
• Type: Conference Papers and Presentations Status: Other Year Published: 2018 Citation: Mulder, P., B. Lingren, C. Bergh, K. Hoelmer and G. Krawczyk. 2018. Developing are-wide approach to management of the brown marmorated stink bug Halyomorpha halys (Stal) in Georgian hazelnuts, a cooperative effort of industry, university and USDA personnel. Entomological Society of America Annual Meeting. Vancouver, B.C. Nov 2018
• Type: Conference Papers and Presentations Status: Other Year Published: 2018 Citation: Peterson, H. M., Ali, J., Krawczyk, G. Exploiting more cues: comparing parasitism of brown marmorated stink bug (Halyomorpha halys Sta?l) sentinel egg masses utilizing different deployment strategies in Pennsylvania fruit orchards. Entomological Society of America Annual Meeting. Vancouver, B.C. Nov 2018
• Type: Conference Papers and Presentations Status: Other Year Published: 2018 Citation: Krawczyk, G., T. Leskey, T. Kuchar, A. Nielsen, C. Hirt and M. Zanelato Nunes. 2018. Brown marmorated stink bug management options for commercial farmers. Global Challenge BMSB (Halyomorpha halys)  International Experience for the Best Solutions. USAID REAP Conference, Tbilisi, Georgia. March 2018
• Type: Websites Status: Published Year Published: 2019 Citation: Updated Insecticide Recommendations for Spotted Lanternfly on Tree Fruit 2018-19. D. Biddinger, H. Leach, J. Urban. https://extension.psu.edu/updated-insecticide-recommendations-for-spotted-lanternfly-on-tree-fruit
• Type: Websites Status: Published Year Published: 2019 Citation: Spotted Lanternfly Management for Homeowners, 2018-19. H. Leach, D. Biddinger, & G. Krawczyk. https://extension.psu.edu/spotted-lanternfly-management-for-homeowners
• Type: Websites Status: Published Year Published: 2019 Citation: Updated Insecticide Recommendations for Spotted Lanternfly on Grape, 2018-19. D. Biddinger, H. Leach, & J. Urban. https://extension.psu.edu/updated-insecticide-recommendations-for-spotted-lanternfly-on-grape
• Type: Other Status: Published Year Published: 2018 Citation: Lewis, J., D. Biddinger, H. Leach, & J. Urban. 2018. Penn state researchers test how to kill spotted lanternflies in Berks county. Reading Eagle, Oct. 10, 2018. https://readingeagle.com/news/article/penn-state-researchers-test-how-to-kill-spotted-lanternflies-in-berks-county
• Type: Journal Articles Status: Published Year Published: 2018 Citation: Pak, D., Biddinger, D., Bj�rnstad, O. 2018. Large scale climate systems, the North Atlantic Oscillation and Arctic Oscillation, influence the spring phenology of Mid-Atlantic tortricid pests across 36 years. Ecological Entomology, DOI:10.1111/een.12712.

Progress 10/01/17 to 09/30/18

Outputs
Target Audience:Target audiences for pollinator work include the 450 fruit growers in Pennsylvania and equivalent numbers in the adjacent mid-Atlantic fruit growing regions of Maryland, Virginia, West Virginia, New York, New Jersey,and North Carolina. Many presentationshave been made at professional meetings to peer scientists, government officials, pesticide industry, and policy makers in various agencies within USDA, including APHIS, NRCS, ARS, OPMP, and NIFA as well as US-EPA. The public was engaged through a large centennial field day at the PSU Research & Extension Station, through workshops with the Xerces Society for Invertebrate Conservation, and PASA (PA Sustainable Agric.) and through several on-line publications through the NE IPM Center, Penn State Center for Pollination Research, Penn State Extension, and the Xerces Society website. Most audiences are aware of problems with pollinators, especially the honey bee, but are not aware of alternative pollinators, how to conserve pollinators with appropriate habitat, and especially the role of pesticides in this decline. We have also reached an international audience of researchers through an international pollinator conference at Penn State and another in Spain. BMSB has become and economic pest in Europe recently and our 4 publications on the adaptation of native biological control agents of Pentatomidae to the invasive BMSB are helping them. Fruit growers and homeowners will recieve updated reccomendations on pesticide impacts and conservation of both honey bees and native bees as well a biological control agents of pests in the upcoming revised 2018-19 edition of the Penn State Tree Fruit Production Guide. This guide has always been available on-line and is considered on of the most complete and effective guides of its type in the US and internationally recognized. The recently invasive pest known as the Spotted Lanternfly found in eastern Pennsylvania has absorbed time and effort of Biddinger & Krawczyk from the fall of 2017 and throughout 2018 as eradication efforts byt the state began to fail and its range increased from 50 square miles to over 6,000 and damage to several vineyards within the quarantine zone became catestrophic. Huge populations of adults were observed feeing in apple orchards for several days in the fall of 2017 & 2018, but damage was minimal. As the pest expands and increases in numbers, their is concern for other agricultural crops such as peach, hops and some vegetables in the future. Probably the most significant economic damage would be to forest trees such as black walnut, maples, and oaks. Research and extension efforts from Biddinger and Krawczyk have been key in in developing pesticide control recommendations from fruit growers and homeowners that are posted on-line at PSU and routinely updated. All work on this pest has to be conducted within the quarentine zone which is about 2 hours from the FREC. Residual pesticide work on grapes and peaches at the PSU Berks campus within the zone have had over a dozen bus tours and the setting for several interviews by local and national news articles on this pest. Krawczyk has been leading effort to develop control recommendations for homeowners utilizing garden store products and in interfacing with grower and the public concerned about the damage, honeydew, and nuisance impact of huge numbers of this mobile pest to homeowners and the public. Changes/Problems:SLF is proving almost impossible to maintain in colonies within the quarentine facilities. Small potted trees or vines do not seem to provide enough sap for long term development of SLF adults or nymphs. The conduct SLF research within the quarentine zone is difficult as it is 3 hours from the PSU campus and 2 hours from the Fruit Research and Extension Center. What opportunities for training and professional development has the project provided?A total of 24 undergraduates, 11 grad students, and 4 post-doctoral scholars were trained in various aspects of pollinator ecology and toxicology, invasive species biology and control, and Integrated Pest and Pollinator Management (IPPM). How have the results been disseminated to communities of interest?Over 30 extension presentations have been made to fruit growers, bee keepers, and the interested public. Several fact sheets on various aspects of SLF biology and control are available to the public at the PSU extension website. Dozens of interviews to trade journals, newspapers, and government agencies have been made on-going SLF research and control ef What do you plan to do during the next reporting period to accomplish the goals?Collaborators will 1) perform research on Spotted Lanternfly (SLF) addressing questions bridging a range of applied to basic aspects of SLF biology, and 2) integrate results from research findings into a strategic management plan of SLF that provides short-term immediate solutions to the current danger of SLF in Pennsylvania, and sustainable long-term solutions to mitigate SLF spread and damage to other locations within the US. Chemical Control: -- To establish efficacy of chemical control in vineyards and orchards -- To evaluate cost effectiveness of various chemical control alternatives -- To develop degree day models to predict spray efficacy -- To test effects of chemical control on secondary pests, and residual contact and ingestion by non-target species (e.g., pollinators) Movement and Monitoring: -- To determine efficacy of establishing trap crop/tree species to slow SLF spread -- To test effectiveness of lures, traps for control and/or monitoring -- To predict dispersal based on adjusted models of Brown Marmorated Stink Bug dispersion (combining natural dispersal and human-assisted dispersal) Damage Potential: -- To assess direct damage from SLF feeding/phloem loss (e.g., reduced yield, winter hardiness, return bloom, ) -- To assess indirect damage from SLF feeding (e.g., sooty mold growth on honeydew, disease vector potential, fireblight, plant susceptibility to secondary pests, wine fault/contamination, etc.) -- To estimate the relative potential for direct and indirect damage induced across four nymphal instar and adult life stages Biology: -- To develop life tables for degree day models to predict hatch and development (including diapause and thermal limits/cold hardiness of eggs) -- To measure dispersal capability of each nymphal instar and adults and build reliable SLF predictive dispersal models -- To determine what host plant(s) are necessary/sufficient for SLF development and production of viable egg cases -- To determine the basis of nutritional requirements/host plant preferences (e.g., high nitrogen, host plant vigor, endosymbiont limitations, etc.) -- To characterize the SLF mating system (e.g., cues, attractants, signaling, parentage, etc.) -- To determine the basis test effectiveness of lures, traps for control and/or monitoring -- To assess basis of direct and indirect damage induced by SLF feeding/phloem loss (e.g., salivary enzymes, manipulation of host plant physiology, characterization of sooty mold, etc. ) Biological Control: -- To characterize and identify exotic biocontrol organisms from native range of SLF -- To evaluate the non-target host range of candidate exotic biocontrol agents -- To characterize and identify potential native biocontrol organisms for SLF -- To test potential biocontrol of Ailanthus altissima with Verticillium nonalfalfae

Impacts
What was accomplished under these goals? 1 & 4. Pesticide evaluations of 42 registered and experimental insecticides/ and acaracides were made on the research station's apple orchards and another 30+ insecticides were evaluated in Berks county to develop spray recommendations for tree fruit and grape growers. A degree day model for determining spray applications for San Jose scale control while minimally impacting biological control by Encarsia perniciosi is being developed and tested on station. 2. Phermone disruption research has been suspended due to the increased priority to develop control recommendations for the new invasive SLF at remote locations and to continue researching the biology and biocontrol of the previous invasive pest, BMSB. 3. Development and evaluations of BMSB monitoring tools across various agro-ecosystems. The practical aspects of various BMSB monitoring and management tools were evaluated within the orchard ecosystem. Multiple trap designs plus various BMSB monitoring lures were evaluated as a tool to decide the necessity of insecticide based management treatments. Development and evaluation of BMSB alternative management systems. The attract and kill method in the form of "ghost traps" was utilized in commercial orchards with very promising results. Additional work to define the exact parameters and economic viability of the methods will need to be conducted in the coming seasons. BMSB populations collected during the late summer period are being utilized to conduct insecticide efficacy and resistance assessments. Brown marmorated stink bug biological control opportunities in managed agricultural systems. Sentinel egg masses are being utilized to evaluate the potential of native biological control agents to impact BMSB eggs, nymphs and adults. We continue the search for the Trisolcus japonicas, the samurai wasp, the most effective egg parasitoid for the BMSB native range in Asia that was found in Pennsylvania for the first time in 2017. A search for native biological control agents against BMSB found several generalist predators and two species of Crabronid wasps that are specialist predators of stink bugs that have quickly adapted to include BMSB as a significant prey item in its diet. Spotted Lanternfly (SLF) - This relatively new invasive species in Pennsylvania has become a significant pest of grape and ornamental trees within the quarentine zone. In addition it is a nuisance pest for homeowners due to its relatively large size, extreme seasonal and local abundance, and sugary honeydew excretion that cause sooty mold to develop. Tree decline in black walnut have been seen in many areas, and near complete loss of grape yield and quality have been noted in several locations and hops appear to be extremely sensitive to feeding. Feeding on apple and peach has been observed in the fall prior to oviposition from extremely high populations, but this feeding seems to last only a several days before they move on to prefered hosts such as grapes. In grape, vines averaging over 200 nymphs have been noted despite increased pesticide applications. Insecticide trials within the quarentine zone were set up in the spring to assess contact and residual activity on SLF nymphs and adults on potted grape and peach a the PSU Berks campus and over 30 insecticides were evaluated on 500 peach and 250 grape vines which resulted in data that was used by pesticide companies resulting in over 10 2(ee) label amendments to include SLF for the first time. This efficacy and residual data was summarized into on-line recommendations for SLF control on grape and on tree fruits. Homeowner recommendations were also developed using data from the fruit trials active ingrediants and several contact and residual trials with specific homeowner products. Various insecticides were also evaluated on SLF overwintering egg masses with only Lorsban being effective. A policy statement cleared by EPA, APHIS and the Pennsylvania Department of Agriculture clarified the use of insecticides on black walnut trees ( a preferred host) as being considered ornamental trees and nut trees in the context of SLF control and allowed the use without restrictions. The use of controlled atmosphere storage used for apple storage with low oxygen and high CO2 was evaluated for its ability to kill eggs on apple bins, but was not effective. Two new fungal pathogens of SLF adults were found to be abundant and are being identified. 5. Pollinators - a survey of apple growers in Pennsylvania and New York was published showing that most do not rely on the honey bee for pollination anymore and rely mostly on wild pollinators for this crop. This is the result of much higher hive rentals over the last 10 years and decreased availability. Testing of orchard insecticides and fungicides has shown that the responses of wild bees and honey bees differ greatly with Osmia being much more sensitive to the ingestion of certain fungicides. Baseline data on pollinator diversity and abundance continues to be collected on a weekly basis in Adams County for assessment of IPPM pesticide mitigation practices in the pollinator communuity. Over 100,000 bees belonging to 238 species from fruit orchards in Adams county have bee collected and data based to serve as a baseline for future research on mitigating pesticide impacts and to document possible declines in bee species dure to other causes. Bioassays have been developed to compare insecticides and fungicide toxicity to adult and larval Osmia cornifrons through ingestion of contaminated pollen or nectar with toxicity to the honey bee. It appears that Osmia are much more sensitive to some fungicides than the honey bee, but not at field realistic doses.

Publications

• Type: Journal Articles Status: Awaiting Publication Year Published: 2018 Citation: Doke, M.A., McGrady, C.M., Otieno, M., Grozinger, C.M., and M. Frazier. "Colony size, rather than geographic origin of stocks, predicts overwintering success in honey bees (Hymenoptera: Apidae) in the northeastern United States" Journal of Economic Entomology (in press)
• Type: Journal Articles Status: Awaiting Publication Year Published: 2018 Citation: Flenniken, M.L. and C.M. Grozinger. Bee Viruses: Ecology, Pathogenicity, and Impacts. Annual Review of Entomology (in press).
• Type: Journal Articles Status: Published Year Published: 2918 Citation: Galbraith, D. A., Z. L. Fuller, A. Brockman, M. Frazier, M. W. Gikungu, K. M. Kapheim, J. T. Kerby, S. D. Kocher, O. Losyev, E. Muli, H. M. Patch, J. M. Sakamoto, S. Stanley, A. D. Vaudo and C. M. Grozinger. "Investigating the viral ecology of global bee communities with high-throughput metagenomics " Scientific Reports 2018 Article #8879.
• Type: Journal Articles Status: Published Year Published: 2018 Citation: Vaudo, A.D., Farrell, L.M., Patch, H.M., Grozinger, C.M. and J.F. Tooker. Consistent pollen nutritional intake drives bumble bee (Bombus impatiens) colony growth and reproduction across different habitats Ecology and Evolution (2018),
• Type: Journal Articles Status: Published Year Published: 2018 Citation: Holt, H.L., Villar, G. and C.M. Grozinger. "Molecular, physiological and behavioral responses of honey bee (Apis mellifera) drones to infection with microsporidian parasites" Journal of Invertebrate Pathology 155, 14-24.(2018)
• Type: Journal Articles Status: Published Year Published: 2018 Citation: Ma, R., Villar, G., Grozinger, C.M., and J. Rangel. Larval pheromones act as colony-wide regulators of collective foraging behavior in honey bees Behavioral Ecology 29(5): 11321141(2018).
• Type: Journal Articles Status: Published Year Published: 2018 Citation: Mu, J., Wu, Q., Yang, Y., Huang, M. and C. M. Grozinger. Plant reproductive strategies vary under low and high pollinator densities Oikos 127: 1081-1094, 10.1111/oik.04711(2018).
• Type: Journal Articles Status: Published Year Published: 2018 Citation: Villar, G., Wolfson, M.D., Hefetz, A.H. and C.M. Grozinger. Evaluating the role of drone-produced chemical signals in mediating social interactions in honey bees (Apis mellifera) J Chemical Ecology 44(1): 1-8 (2018).
• Type: Journal Articles Status: Published Year Published: 2017 Citation: Levin, S., Galbraith, D., Sela, N., Erez, T., Grozinger, C.M., and N. Chejanovsky. Presence of Apis rhabdovirus-1 in populations of pollinators and their parasites from two continents Frontiers in Microbiology 12 December 2017 https://doi.org/10.3389/fmicb.2017.02482.
• Type: Journal Articles Status: Published Year Published: 2017 Citation: Rivera Vega, L., Galbraith, D.A., C.M. Grozinger and G. W. Felton. "Host plant driven transcriptome plasticity in the salivary glands of the cabbage looper (Trichoplusia ni)" PLoS ONE 12(1): e018636 (2017).
• Type: Journal Articles Status: Published Year Published: 2017 Citation: Amsalem, E. and C. M. Grozinger. Evaluating the molecular, physiological and behavioral impacts of CO2 narcosis in bumble bees (Bombus impatiens). Journal of Insect Physiology 101:57-65 (2017).
• Type: Journal Articles Status: Published Year Published: 2017 Citation: Amsalem, E.*, Padilla, M.*, Schreiber, P.M. #, Altman, N., Hefetz, A., and C.M. Grozinger. "Do bumble bee (Bombus impatiens) queens signal their reproductive and mating status to their workers?" Journal of Chemical Ecology 43(6): 563-572 (2017), * indicates equal contribution, # denotes undergraduate researcher
• Type: Journal Articles Status: Published Year Published: 2017 Citation: McMenamin, A.*, Mumoki, F.*, Frazier, M., Kilonso, J., Mweu, B., Baumgarten, T., Patch, H., Torto, B., Masiga, D., Tumlinson, J., Grozinger, C.M., and E. Muli. "The impact of hive type on the behavior and health of honey bee colonies (Apis mellifera scutellata) in Kenya" Apidologie 48(5): 703-715(2017).
• Type: Journal Articles Status: Published Year Published: 2017 Citation: Geffre, A.C., Liu, R., Manfredini, F., Beani, L., Kathirithamby, J., Grozinger, C.M., and A. L. Toth. Transcriptomics of an extended phenotype: parasite manipulation of wasp social behaviour shifts expression of caste-related genes. Proc Roy Soc B 284(1852):20170029 (2017).
• Type: Journal Articles Status: Published Year Published: 2017 Citation: Villar, G. and C. M. Grozinger. "Primer Effects of the Honey Bee Queen Pheromone 9-ODA on Drones (Apis mellifera)" Animal Behavior 127: 271-279 (2017).
• Type: Journal Articles Status: Published Year Published: 2017 Citation: Doublet, V.*, Poeschl, Y.*, Gogol-D�ring, A., Alaux, C., Annoscia, D., Aurori, C., Barribeau, S.M., Bedoya-Reina, O., Brown, M.J.F., Bull, J.C., Flenniken, M.L., Galbraith, D.A., Genersch, E., Gisder, S., Grosse, I., Holt, H.L., Hultmark, D., Lattorff, H.M.G., Le Conte, Y., Manfredini, F., McMahon, D.P., Moritz, R.F.A., Nazzi, F., Ni�o, E.L., Nowak, K., van Rij, R.P., Paxton, R.J.*, and C. M. Grozinger*. "Unity in defence: honeybee workers exhibit conserved molecular responses to diverse pathogens" BMC Genomics 18(1): 207 (2017). *indicates co-first authors and co-senior authors.
• Type: Journal Articles Status: Published Year Published: 2018 Citation: Park, M., Joshi, N., Rajotte, E., Biddinger, D., Losey, J., & Danforth, B. (2018). Apple grower pollination practices and perceptions of alternative pollinators in New York and Pennsylvania. Renewable Agriculture and Food Systems, 1-14. doi:10.1017/S1742170518000145 .
• Type: Journal Articles Status: Published Year Published: 2017 Citation: Hayek, A. E., L. F. Solter, J. V. Maddox, W. F. Huand, A. S. Estep, G. Krawczyk, D. C. Weber, N. D. Sanscrainte and J. J. Becnel. 2017. Nosema maddoxi sp. nov. (Microsporidia, Nosematidae), a widespread pathogen of green stink bug Chinavia hilaris and the brown marmorated stink bug, Halyomorpha halys (Stal). J. Eukaryotic Microbiology 65: 315-330, doi:10.1111/jeu.12475
• Type: Journal Articles Status: Published Year Published: 2018 Citation: Mujica, V., M. Preti, E. Basoalto, L. Cich�n, E. Fuentes-Contreras, W. Barros-Parada, G. Krawczyk, M. Z. Nunes, J. Walgenbach, R. Hansen and A. Knight, 2018. Improved monitoring of oriental fruit moth (Lepidoptera: Tortricidae) with terpinyl acetate plus acetic acid membrane lures. Journal of Applied Entomology, doi: 10.1111/jen.12528
• Type: Journal Articles Status: Accepted Year Published: 2018 Citation: Morrison, W., B. Blaauw, B. Short, A. Nielsen, C. J. Bergh, G. Krawczyk, Y-L. Park, B. Butler, A. Khrimian, and T. Leskey. 2018. Successful management of Halyomorpha halys (Hemiptera: Pentatomidae) in commercial apple orchards with an attract-and-kill strategy. Pest Management Science. doi:10.1002/ps.5156

Progress 02/02/17 to 09/30/17

Outputs
Target Audience:Target audiences include the 450 fruit growers in Pennsylvania and equivalent numbers in the adjacent mid-Atlantic fruitgrowing regions of Maryland, Virginia, West Virginia, New York, New Jersey,and North Carolina. Many presentations have been made at professional meetings to peer scientists, government officials, pesticide industry, and policy makers in various agencies within USDA, including APHIS, NRCS, ARS, and NIFA as well as EPA. The public has been engaged through large field days at the PSU Research Station, through workshops with the Xerces Society and PASA (PA Sustainable Agric.) and several on-line publication through the NE IPM centers, Penn State Center for Pollination Research, USDA-NRCS publications, and the Xerces Society website. Most audiences are aware of problems with pollinators, especially the honey bee, but are not aware of alternative pollinators, how to conserve pollinators with appropriate habitat, and especially the role of pesticides in this decline. We have also reached an international audience of researchers through an international pollinator conference at Penn State and another in Spain. BMSB has become and economic pest in Europe recently and our 4 publications on the adaptation of native biological control agents of Pentatomidae to the invasive BMSB are helping them. Fruit growers and homeowners will recieve updated reccomendations on pesticide impacts and conservation of both honey bees and native bees as well a biological control agents of pests in the upcoming revised 2018-19 edition of the Penn State Tree Fruit Production Guide. This guide has always been available on-line and is considered on of the most complete and effective guides of its type in the US and internationally recognized. Presentations were made to 320 high school students and instructors from 47 states, 7 Canadian provinces, and China on biodiversity, conservation biological control, and pollinator diversity as part of the 2017 National Conservation Foundation Envirothon. Changes/Problems:Spotted Lanternfly has been added as newly invasive pest of fruit crops and forestry in Pennsylvania and we are forming a response team to research short- and long-term solutions to this pest including pesticides and biological control. What opportunities for training and professional development has the project provided?Two Ph.D students are currently being trained in tree fruit IPM and pollinator conservaton in fruit orchards at the Fruit Research Lab. Additionally 7 graduate students and 3 post-docs are being trained in pollinator physiology and conservation in laboratories on the main campus. How have the results been disseminated to communities of interest?Many workshops, symposia, and oral presentations have been given on tree fruit IPM, conservation biological control,pollinator decline and conservation, CCD and the role of pesticides and co-formulant surfactants on pollinator health, at local, state, regional, national, and international levels. On line publications, technical bulletins, technical specifications for NRCS, and YouTube videos have been made available to the public. What do you plan to do during the next reporting period to accomplish the goals?Bees - We will continue determine exposure levels and timing to neonicotinoid and other insecticides on honey bees and wild bees and use this information to mitigate impacts or to utilize safer alternatives in our conventional IPM programs that usually focus on biological control of pests. We will look at long-term sublethal effects of pesticides in pollen to Osmia and honey bees in an attempt to develop aggregate dose measures that go beyond exposure at the single flower level and examine more closely oral exposure between several different bee species and the effects of sublethal, field relevant doses on behavior, development and reproduciton. We will attempt to determine the economic value of multiple species of solitary bees and to what extent they can supplement or even replace honey bees as tree fruit pollinators. Future work will concentrate on pesticide toxicity and sublethal reproductive effects through ingestion of contaminated pollen or nectar since we believe this to be the mostly likely route of exposure in tree fruit systems. Pesticide testing will continue to evaluate new and old products in order to develop more ecologically-based IPM programs that minimize pesticide use and relies more on natural controls or targeted systems like pheromone mating disruption of pest specific viruses or nematodes. Invasive Species (BMSB, SLF) - will continue as major effort to better understand basic biology, pests status, host range and seasonal development, and biological control in order to minimize the economic impacts of these new pests in PA agriculture.

Impacts
What was accomplished under these goals? The results from a cooperative fruit grower survey from NY and PA demonstrates that the majority of apple growers in these states are no longer using honey bees for pollination, but rather are relying on the 50+ species of wild bees that we have found pollinating fruit trees. This is potentially saving apple growers up to $200/acre in honey bee hive rental. This work represents one of the few documented instances of wild pollinators carrying out most of a specialty crop's pollination needs. Three years of surveying the pollinator communities in fruit orchards with those found in USDA-NRCS funded pollinator enhancement strips of wild flowers demonstrates that these diversified floral plantings increase tree fruit pollinator diversity and abundance by providing additional food resources for important bee species after fruit bloom. With regards to orchard management practices, the impacts on the orchard pollinator communities of a reduced risk IPM program relying on neonicotinoids and other new pesticide chemistries with conventional programs consisting mostly of broad spectrum organophosphate insecticides found no differences. Standardized methods were also developed to passively sample and assess pollinator populations over time. Blue vane traps and colored water pan traps with active net collections of pollinators at bloom in orchards were compared to determine species declines and to assess the effectiveness of best management practices in orchards under differing pest management programs. Other work assessed the indigenous arthropod natural enemies of the invasive brown marmorated stink bug (BMSB) in Pennsylvania as part of a comprehensive review of BMSB in North America and Europe. In addition, we are leading the applied research efforts at Penn State in developing control methods for the newly invasive Spotted Lanternfly on tree fruits and grapes with pesticides and natural enemies. In conjunction with the Xerces Society for Invertebrate Conservation we published a comprehensive 44 page review of the literature assessing the impacts of neonicotinoid insecticides on bees available online at: http://xerces.org/neonicotinoids-and-bees/.The previous version had over 150,000 downloads and is extensively cited. As part of FAO book entitled The Pollination of Cultivated Plants: A Compendium for Practioners, we published a chapter on Integrating pollinator health into tree fruit IPM - a case study of Pennsylvania apple production. A Penn State Extension circular developed jointly with the Xerces Society - Managing Northeast Apple Orchards for Pollinators and Oher Beneficial Insects: Integrated Pest Management, Habitat Enhancement, and Manage Bees. Over 20 Extension presentations and workshops were given on tree fruit IPM programs to economically control pests while still conserving biological control and pollinators.

Publications

• Type: Journal Articles Status: Accepted Year Published: 2017 Citation: Joshi, N. K., T. Leslie, E. Rajotte and D. Biddinger. 2017. Environmental impacts of reduced-risk and conventional pesticide programs differ in commercial apple orchards, but similarly influence pollinator community. Chemosphere. (accepted 9/10/17).
• Type: Journal Articles Status: Accepted Year Published: 2017 Citation: Biddinger, D. & N. Joshi. 2017. First report of native Astata unicolor (Hymenoptera: Crabronide) predation on the nymphs and adults of the invasive brown marmorated stink bug, Halyomorpha halys (Hemiptera: Pentatomidae) (in press). Florida Entomologist.
• Type: Journal Articles Status: Published Year Published: 2017 Citation: Abram, P. K., K. A. Hoelmer, A. Acebes-Doria, H. Andrews, E. H. Beers, J. C. Bergh, R. Bessin, D. J. Biddinger, et. al. 2017. Indigenous arthropod natural enemies of the invasive brown marmorated stink bug in North America and Europe. Journal of Pest Science. doi:10.1007/s10340-017-0891-7. pp 1-12.
• Type: Journal Articles Status: Published Year Published: 2017 Citation: Gibbs, J., N. K. Joshi*, J. Wilson, N. Rothwell, K. Powers, M. Haas, L. Gut, D. Biddinger, and R. Isaacs. 2017. Does passive sampling accurately reflect the bee (Apoidea: Anthophila) communities pollinating apple and sour cherry orchards? Environmental Entomology 46(3):579-5988. https://doi.org/10.1093/ee/nvx069 .
• Type: Journal Articles Status: Published Year Published: 2017 Citation: Biddinger D., A. Surcic?, and N. K. Joshi*. 2017. A native predator utilizing the invasive brown marmorated stink bug, Halyomorpha halys (Hemiptera: Pentatomidae) as a food source. Biocontrol Science and Technology. https://doi.org/10.1080/09583157.2017.1354247.
• Type: Book Chapters Status: Awaiting Publication Year Published: 2017 Citation: Biddinger, D., E. G. Rajotte, N. K. Joshi. 2017. Integrating pollinator health into tree fruit IPM- A case study of Pennsylvania apple production (Chapter- 4), p. 143-149. In: The pollination of cultivated plants: a compendium for practitioners. Vol. 1. (Editor- D. Roubik). Food and Agricultural Organization of the United Natons. (In Press). 313 p.
• Type: Conference Papers and Presentations Status: Published Year Published: 2017 Citation: Joshi N.K. and Biddinger D.J. (2017). Nest modification of the Japanese orchard bee (Osmia cornifrons) protects its developmental stages from a cleptoparasitic mite pest. Ecological Society of America Annual Meeting. https://eco.confex.com/eco/2017/webprogram/Paper69506.html
• Type: Journal Articles Status: Accepted Year Published: 2017 Citation: Shugrue, S., Joshi, N. K., Leslie, T., Rajotte, E., and D. Biddinger. Diversified floral resource plantings support bee communities after apple bloom in commercial orchards. Nature Scientific Reports. (accepted Oct. 2017)
• Type: Books Status: Awaiting Publication Year Published: 2017 Citation: J. Hopwood, D. Biddinger, K. Gill, M. Vaughan, E. Lee-Mader, A. Code, N. Joshi, and E. Rajotte. (2017 in press). Managing Northeast Apple Orchards for Pollinators and Other Beneficial Insects: Integrated Pest Management, Habitat Enhancement and Managed Bees. Penn State University and Xerces Society for Invertebrate Conservation Joint Publication, 55 p.
• Type: Conference Papers and Presentations Status: Other Year Published: 2017 Citation: D. Biddinger*, E. Rajotte, & N. Joshi. IPPM: Managing crop pests and pollinator health simultaneously. Pennsylvania State University Center for Pollination Research Spring Symposium, State College, PA. May 23, 2017.
• Type: Conference Papers and Presentations Status: Other Year Published: 2017 Citation: Phan, N.*, D. Biddinger, & E. Rajotte. Impact of pesticides on Osmia and honey bees. Pennsylvania State University Center for Pollination Research Spring Symposium, State College, PA. May 23, 2017.
• Type: Other Status: Other Year Published: 2017 Citation: D. Biddinger. Invited Seminar. Developing integrated pest and pollinator management strategies in apple orchards and cranberry bogs. University of Massachusetts Cranberry Research Station, E. Wareham, MA. March 23, 2017.
• Type: Other Status: Other Year Published: 2017 Citation: D. Biddinger. Invited Seminar. Integrated pest and pollinator management in Pennsylvania orchards. Dept. of Entomology, Michigan State University, East Lansing, MI. Feb. 27, 2017.
• Type: Other Status: Published Year Published: 2017 Citation: Scully, T. and D. Biddinger. 2017. Why orchard biocontrols are naturally effective. Growing Magazine. August 14, 2017. https://www.growingmagazine.com/fruits/orchard-biocontrols-naturally-effective/
• Type: Other Status: Published Year Published: 2017 Citation: Colby, S. and D. Biddinger. 2017. Encouraging native pollinators in apple orchards. Growing Magazine. July 1, 2013. https://www.growingmagazine.com/fruits/encouraging-native-pollinators-in-apple-orchards/
• Type: Other Status: Published Year Published: 2017 Citation: K. Ulman, D. Biddinger, & M. Vaughan. 2017. Pennsylvania apple pollination. http://icpbees.org/wp-content/uploads/2016/05/PA-Apple-Pollination-Factsheet-Final.pdf
• Type: Other Status: Published Year Published: 2017 Citation: D. Biddinger & T. Baugher. 2017. Natural enemies/biological control in orchards. http://extension.psu.edu/plants/tree-fruit/insects-mites/natural-enemies-and-controls/natural-enemies-biological-control-in-orchards
• Type: Other Status: Published Year Published: 2017 Citation: D. Biddinger & T. Baugher. 2017. Toxicity of pesticides to mite and aphid predators. http://extension.psu.edu/plants/tree-fruit/insects-mites/natural-enemies-and-controls/toxicity-of-pesticides-to-mite-and-aphid-predators
• Type: Theses/Dissertations Status: Published Year Published: 2017 Citation: Sarah Shugrue. MS thesis. 2017. Pesticide use, habitat manipulation and management changes as factors in pollinator sustainability in Pennsylvania apple orchards. 75 p. Biddinger thesis advisor.
• Type: Journal Articles Status: Accepted Year Published: 2017 Citation: Annoscia, D., Zanni., V., Galbraith, D., Quirici, A., Grozinger, C., Bortolomeazzi, R., Nazzi, F. Elucidating the mechanisms underlying the beneficial health effects of dietary pollen on honey bees (Apis mellifera) infested by Varroa mite ectoparasites. Scientific Reports 7: 6258(2017).
• Type: Journal Articles Status: Published Year Published: 2017 Citation: Zanni., V., Galbraith, D., Annoscia, D., Grozinger, C.M., Nazzi, F. Transcriptional signatures of parasitization and markers of colony decline in Varroa-infested honey bees (Apis mellifera). Insect Biochemistry and Molecular Biology 87: 1-13. (2017)
• Type: Journal Articles Status: Published Year Published: 2017 Citation: Kuhar, T., B. Short, G. Krawczyk, & T. Leskey. 2017. Deltamethrin-incorporated nets as an integrated pest managment tool for the invasive Halyomorpha halys (Hemiptera:Pentatomidae). 110(2): 543-545.
• Type: Journal Articles Status: Published Year Published: 2017 Citation: Nielsen, A., S. Fleischer, G. Hamilton, T. Hancock, G. Krawczyk, J. Lee, E. Ogburn, J. Pote, A. Raudenbush, A. Rucker, M. Saunders, V. Skillman, J. Sullivan, J. Timer, J. Walgenbach, N. Wiman, & T. Leskey. 2017. Phenology of brown marmorated stink bug described using female reproductive development. Ecology and Evolution 7(17): 1-11.
• Type: Journal Articles Status: Published Year Published: 2017 Citation: Evans, K., N. Ostiguy, & M. Lopez-Uribe. 2017. Efficacy of different methods of oxalic acid application. American Bee Journal 157(5): 505-507.
• Type: Journal Articles Status: Published Year Published: 2017 Citation: Lopez-Uribe, M., A. Fitzerald, & M. Simone-Finstrom. 2017. Inducible versus constitutive immunity: Examining effects of colony infection on glucose oxidase and defensin-1 production in honey bees. Royal Society Open Science 4(5): 170-224.
• Type: Journal Articles Status: Published Year Published: 2017 Citation: Lopez-Uribe, A. Soro, & S. Jha. 2017. Conservation genetics of bees: advances in the application of molecular tools to guide bee pollinator conservation. Conservation Genetics 18:501506 DOI 0.1007/s10592-017-0975-1
• Type: Journal Articles Status: Published Year Published: 2017 Citation: L�pez-Uribe MM, Appler RH, Dunn RR, Frank SD, Tarpy DR. (2017) Higher immunocompetence is associated with higher genetic diversity in feral honey bee colonies (Apis mellifera). Conservation Genetics. doi: 0.1007/s10592-017-0942-x.