Source: PENNSYLVANIA STATE UNIVERSITY submitted to
SUSTAINABLE SOLUTIONS TO PROBLEMS AFFECTING BEE HEALTH
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
REVISED
Funding Source
Reporting Frequency
Annual
Accession No.
1020527
Grant No.
(N/A)
Project No.
PEN04716
Proposal No.
(N/A)
Multistate No.
NC-_old1173
Program Code
(N/A)
Project Start Date
Nov 21, 2019
Project End Date
Sep 30, 2024
Grant Year
(N/A)
Project Director
Grozinger, CH, M.
Recipient Organization
PENNSYLVANIA STATE UNIVERSITY
208 MUELLER LABORATORY
UNIVERSITY PARK,PA 16802
Performing Department
Entomology
Non Technical Summary
Insect pollinators provide essential pollination services to growers of U.S. fruits, vegetables, nuts and seeds. Honey bees are the premier managed pollinators of most crops, accounting for $11.7 billion of the $15 billion of agricultural output attributable to insect-mediated pollination. To satisfy the demand for pollination, about 2 million of the 2.6 million managed honey bee colonies in the U.S. are rented and placed in nearly 100 different crops each year.Efficient delivery of managed pollination services is threatened by the poor state of U.S. honey bees. Since the mid-2000s beekeepers have consistently experienced annual colony losses of 31-46%. While beekeepers can often make up for these losses through intensive management of surviving colonies, current management tools are costly and may not be sufficient to indefinitely sustain the honey bee colony numbers or colony strength needed for pollination. Other managed pollinators such as the alfalfa leafcutting bees and unmanaged wild pollinators also contribute substantially to agricultural pollination in many crops. Unfortunately, the long-term health and abundance wild pollinators is also under threat.The causes of honey bee and pollinator declines in the U.S. are varied, complex, and defy a simplistic explanation, as multiple stressors are almost certainly involved. Significant progress in identifying contributing factors to bee declines has been made by many current members of the NC1173 multi-state project through collaborative programs. Previous collaborations include a $4.1M, 4-year USDA CAP project to study the causes of Colony Collapse Disorder (CCD) and other factors affecting bee populations; and a $5M CAP project through the USDA Global Food Security program to establish the Bee Informed Partnership, an extension-only effort to collect and disseminate information about the health of the managed honey bee population.Many of the findings from these large collaborative and multistate projects were presented and synthesized at the Stakeholders Conference on Honey Bee Health convened by the USDA and the U.S. Environmental Protection Agency in October 2012. The summary of this conference provided a roadmap for future research and priority areas listed below continue to be relevant and are being addressed by members of the NC1173 multi-state project.Biotic FactorsParasites, Pests and Pathogens. The parasitic mite, Varroa destructor, and the viruses it helps to transmit, remain a top concern for beekeepers. The gut microsporidian pathogen Nosema spp. has been implicated in honey bee colony losses and in managed and wild bumble bees. A range of other bacteria, fungi, and pests negatively affect bee health, particularly when colonies are at a weakened or immunosuppressed state. Improved understanding of the interaction between bees and their parasites, pests, and pathogens will yield better management and control strategies.Breeding and genetic diversity. Breeding resistance to parasites and pathogens in bees is a long-term sustainable approach to mitigate colony losses, and stock improvement is an ongoing effort supported by industry, USDA and University programs.Recent inclusion of the honey bee in the USDA National Animal Germplasm Program has resulted in cryogenic conservation of honey bee germplasm from original source populations in the Old World and commercial strains within the US.Additionally, research on and applied efforts to maintain the genetic diversity of honey bee populations and improve mating success of queen honey bees under commercial production play important roles in pollination security.Abiotic FactorsForage availability and nutritional stress. The nutritional requirements of honey bees and other pollinators are not met by the floral landscape in some parts of the U.S. Research is needed to examine land- and farm-management practices associated with high levels of colony and pollinator success.Pesticides and environmental contaminants. Insecticides designed to kill insects may also harm pollinating insects. Other pesticides and environmental contaminants also have the potential to adversely affect individual bees and colony development. Additionally, drugs used to control pathogens may have unintended side effects. Therefore, more work is needed to determine the effects of pesticide exposure on colony health, honey production and delivery of pollination services. Development and delivery of beekeeper practice recommendations that incorporate integrated pest management principles may reduce unintended side-effects and further stress on colonies.The consensus is that these multiple biotic and abiotic stressors, working in concert, are responsible for the honey bee and pollinator health issues currently manifested in the U.S. While advances are being made in all these key research areas, a real solution to honey bee and pollinator health will come through a combined broad approach, a task that is too big and complex to be managed by individual researchers. As such, the collaborative work fostered by the NC1173 multi-state research project is critical to building a holistic understanding of honey bee and pollinator health. There is a clear need defined by stakeholders to mitigate the continued decline of honey bees and other insect pollinators. The consequences of inaction are a further destabilized food-production system, decreased yields and quality of fruits and vegetables, and potentially higher produce prices. The technical feasibility of the proposed working group is greatly facilitated by the existing practice of adjoining the American Bee Research Conference (ABRC), the annual professional meeting of the American Association of Professional Apiculturists (AAPA), with one of the three national apiculture associations in the U.S. in alternating years: the American Beekeeping Federation (ABF), the American Honey Producers of America (AHPA), and the Apiary Inspectors of America (AIA). This tradition of interfacing with clientele and other professional groups involved in beekeeping is ideally suited to collaboration, interaction, and discussion of current and emerging issues regarding honey bee health. Thus, there is a clear advantage of fostering this multi-state effort, because there is great similarity in the threats to American beekeeping across all regions. The impacts from these ongoing interactions have been significant (see above), and therefore, a continuation of the NC1173 working group will advance these successes going forward. We should note that a CRIS search was conducted for the expiring NC1173 project, so there is no overlap with any ongoing projects.
Animal Health Component
100%
Research Effort Categories
Basic
60%
Applied
20%
Developmental
20%
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
2113010106050%
2113085106040%
2113095106010%
Goals / Objectives
To evaluate the role, causative mechanisms, and interaction effects of biotic stressors (i.e. parasitic mites, pests, and pathogens) and abiotic stressors ((i.e. exposure to pesticides, poor habitat and nutrition, management practices) on the survival, health and productivity of honey bee colonies as well as within pollinator communities. To facilitate the development of honey bee stock selection, maintenance and production programs that promote genetic diversity and incorporate traits conferring resistance to parasites and pathogens. To develop and recommend "best practices" for beekeepers, growers, land managers and homeowners to promote health of honey bees and pollinator communities.
Project Methods
These studies involve a combination of laboratory and controlled field studies, as well as data collected from field studies conducted at large spatiotemporal scales and with data collected from citizen scientists. Highlights of methods for projects to address specific objectives are provided below.Objective 1. Grozinger, Hines, Lopez-Uribe, Patch, Rajotte, Hoover, BoyleWe are examining the epidemiology of bee pathogens in insect communities. In this large-scale project we are screening bee communities in sites across central Pennsylvania for a panel of known bee pathogens to address the following questions: 1) Do pathogens have different prevalence in bees that differ in sociality and community interactions? 2) How are pathogens circulated within and between bee and non-bee species? 3) How are pathogens within these bees predicted by the community of pathogens present on flowers? 4) Is there a seasonality to pathogen prevalence? 5) How do pathogens flow across the landscape? Together all of these data will allow us to build a model for pathogen spread and provide a holistic understanding of how pathogens can impact communities.In our previous USDA-funded studies, we found that bumble bee foraging preferences are shaped by macronutrient ratios, such that bees preferentially foraging for pollen with a specific protein:lipid ratio (Vaudo et al 2016a, 2016b) . With funding from the USDA-SCRI, we have evaluated the attraction of diverse pollinators to annual and perennial ornamental plant stocks (5 species of annuals, 5 species of perennials, 5 species/cultivar). We have documented significant variation in visitation patterns among species and cultivars, and found a significant effect of season, year, and site. We are now evaluating the role of floral traitsin shaping these interactions.We have found that pollen diets improve bee resilience to pesticides, pathogens and parasites. We are now conducting controlled laboratory studies in different bee species to examine the impact of dietary pollen and pollen macronutrients on bee health and resilience.We are examining the impact of nutrition and rearing conditions on various metrics of bumble bee health. This project is near completion and has revealed that pollen nutrition has the largest effect on bee health and bee coloration although climate plays a role, and that bee coloration is a potential bioindicator of the nutritional quality available to bees in natural landscapes.We have launched a new program, Beescape, to collect data from (1) field samples of wild bees (2) networks of participating beekeepers (3) networks of participating gardners. The results of these studies are incorporated into models using data on landscape forage quality, nesting habitat, pesticide use,weather conditions as well as beekeeper management practices to identify the factors that best predict health outcomes. We have developed an online portal (beescape,org) to dissemination informaiton and gather data from citizen scientists.Finally, we have estimated the surprisingly large diversity bees in agroecosystems, evaluated the role of landscape in shaping pollinator communities and influencing pollination services in agroecosystems, and created pollinator habitat and assessed its impacts on bee communities and pollination services.Objective 2. Lopez-Uribe, Grozinger, BoyleFeral (unmanaged) honey bees appear to be more resilient to pathogens and parasites then their managed counterparts. We are examining the role of genetics and environment (management) on this resilience. We demonstrated that higher immunocompetence in feral bees is associated with higher genetic diversity (Lopez-Uribe et al 2017) and received funding from USDA Animal Health program to compare disease levels and immunocompetence in feral and managed honey bee colonies in Pennsylvania, using a citizen-science approach (http://lopezuribelab.com/tracking-feral-bee-health/).We are working with Jason Rasgon (PSU) to develop methods for genetic transformation of bees, which will facilitate the identification and validation of genetic markers for bee health and behavior; this project was been funded by a grant USDA Exploratory Research program, the USDA Postdoctoral Fellows program, and the NSF-EDGE program. We have worked with members of the PA Queen Improvement Project to help them analyze data from their comparisons of Varroa resistant honey bee stocks.Objective 3. Grozinger, Lopez-Uribe, Patch, Rajotte, Hoover, BoyleProject COMB (Conventional and Organic Management of Bees)aims to determine the impacts of various management systems on honey bee colony health. Specifically, our goal is to do a side-by-side comparison ofconventional,organic, andchemical freemanagement systems to determine how beekeeping practices impact colony health and productivity, disease and pest tolerance, and how all of these factors impact beekeeping economics. In November 2017, we met with 27 stakeholders, ranging from hobbyists to commercial beekeepers,to develop the protocols for each management system based on their current practices. In April 2018, we will begin the experiment with the establishment of 288 colonies; 216 in Pennsylvania and 72 in West Virginia (see locations on map).Colonies will be managed and followed for two years. To measure colony health, we willsample colonies for various diseases and pests,includingvarroa mites, nosema, and various viruses. We will also measure and monitor colony status using metrics suchas comb building, honey production, swarming behavior, bee immunity, and pesticide exposure. In addition, we will conduct an economic analysis quantitatively compare the costs and benefitsof the different management systems.Our long-term goals are (1) to provide beekeepers with scientific information that helps them make informed decisions about their beekeeping practices, and (2) create standardized protocols for organic beekeeping management, which can support the development of a new market for organic honey bee products in the United States.We worked together with a team of 36 individual representing 28 state- and national-organizations and stakeholder groups to develop the Pennsylvania Pollinator Protection Plan (P4): http://ento.psu.edu/pollinators/research/the-pennsylvania-pollinator-protection-plan-p4 It summarizes the current state of pollinators in Pennsylvania, and provides recommendations for best practices and resources to support and expand pollinator populations. The P4 focuses on best practices for forage and habitat, pesticide use, and beekeeping in urban, agricultural, natural and roadside habitats.Integrated Pest Management (IPM) is a long standing, science based, decision making process whose ecological roots lie in the use of multiple biological, cultural, physical, and chemical tactics to protect crops in a way that minimizes economic, health, and environmental risks. IPM can address any pest complex (insect, disease, weed, vertebrate, etc.) and can be adapted to any agricultural production goals including conventional, sustainable and organic. IPM can be adjusted to protect pollinator health just as it is adjusted to protect other beneficial organisms such as predators and parasitoids. In an Integrated Pest and Pollinator Management (IPPM) context, both pest management and pollinator protection may be achieved. We have a number of projects in apple, pumpkin and cotton agroecosystems in which we apply this approach.

Progress 11/21/19 to 09/30/20

Outputs
Target Audience:Our target audience includes beekeepers, growers, land managers, members of the public, policymakers, and the scientific community. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?Through this HATCH project, numerous undergraduate students, graduate students and postdoctoral fellows are being trained. We obtained funding for a graduate training program in Integrative Pollinator Ecology (IPE) through funding from the Penn State College of Agricultural Sciences Strategic Initiative Program, the Huck Institutes of the Life Sciences and the USDA NNF program. The IPE program trains graduate Fellows to holistically tackle issues in pollinator health and ecology. Fellows will develop integrative research, education and outreach programs that span multiple disciplines - from genomics to land management - and interface with diverse stakeholder groups. The PIs teach numerous undergraduate and graduate degree courses on honey bees and pollinators, including a general education course, ENT 222, "Honey Bees and Humans" which reaches 70 students annually from across the university (Patch and Grozinger). In the integrated pest management course ENT 457, pollinator protection is discussed as a key IPM goal (Rajotte). In fall 2020, we launched a joint course with the University of Freiburg, "Global Perspectives in Integrated Pest and Pollinator Management,"led by Boyle and Grozinger, and including lectures from Rajotte. How have the results been disseminated to communities of interest?We connect with diverse audiences through multiple venues, outlined below, ensuring that the information generated from our research efforts are rapidly disseminated. PA Pollinator Protection Plan (all faculty members, led by Boyle). We worked together with a team of 36 individuals representing 28 state- and national-organizations and stakeholder groups to develop the Pennsylvania Pollinator Protection Plan (P4). Dr. Natalie Boyle organizes meetings of the P4 group every four months. The Center for Pollinator Research website (all faculty members, led by Boyle). The Center website received >100K views a year. Boyle recently led a restructuring of the website content. Pollinator Webinar Series (led by López-Uribe with contributed seminars from Boyle and Grozinger). The Pollinator Webinar Series Summer 2020 had a total of 7,351 people registered. Participants joined from 16 countries, all states in the United States, and all but one county in Pennsylvania. The webinar series included eight topics related to pollinator biology, ecology, and management. The Pennsylvania Tree Fruit Production Guide has been modified to accommodate pollinator health under an IPPM strategy. Pesticide recommendations including active ingredients, application rates and application timings have been adjusted to protect pollinators while maintaining economic pest control in tree fruit crops. Stakeholder Groups. The Center for Pollinator Research's Stakeholder Advisory Board consists of regional and national representatives of grower, beekeeper, industry, and nonprofit groups. The Board meets together with the P4 group (above). Public. Each year, we participatein several science fairs, including the Great Insect Fair (Department of Entomology) and PA Ag Progress Days. These events reach >10,000 individuals annually. K-12 students. With Penn State's Center for Science and the Schools, we received funding from the USDA-PD-STEP program to develop programming targeting K-12 teachers from underserved rural and urban communities. We created lesson plans and other content that are available online (Grozinger, Patch, Boyle). With faculty in Penn State's Learning, Design and Technology Program we developed a one-hour workshop for families with pre-K through middle school children for use in rural libraries and museums (Grozinger). We have conducted several school visitsand presentations as part of the PSU "Nature Explorers" summer camp (elementary school) and the Pennsylvania School of Excellence in Agricultural Sciences high school summer program (Hines). Undergraduate students. We work with Penn State's undergraduate Beekeeping Club, and support student training as part of several projects across our research groups. The PIs teach numerous undergraduate and graduate degree courses on honey bees and pollinators, including a general education course, ENT 222, "Honey Bees and Humans" which reaches 70 students annually from across the university. In the integrated pest management course ENT 457, pollinator protection is discussed as a key IPM goal. We administer the Apes Valentes Award, which is awarded annually to select undergraduate or graduate students in the sciences, arts, and humanities, to perform pollinator-related summer projects. Beekeepers. We regularly present at and play a leadership role in local, regional and national beekeeper conferences;and students often receive awards from several of these organizations. Lopez-Uribe co-organizes the PA State Beekeepers Association meetings in November. We host two citizen-scientist projects with beekeepers in Pennsylvania and surrounding states: "Tracking Feral Bees" and "Beescape." Finally, in 2020 we created a series of extension notes, which provide support for diagnosing and managing bee diseases and for honey bee queen rearing. Gardeners and land managers. We work closely with the Penn State Master Gardeners, the USDA-NRCS, and the Xerces Society to develop recommendations and planting schemes for improving nesting habitat and the abundance and diversity of flowering plant species to support the nutritional needs of pollinators. We are working with the Penn State Sustainability Institute to develop best practices for developing pollinator habitat and forage at solar array sites, using 500 acres of solar farms under construction at Penn State at model sites. The Master Gardeners have developed a highly successful "Pollinator Garden Certification Program,"and have certified hundreds of gardens throughout the state. With the Xerces Society and USDA-NRCS, we have created technical bulletins, popular publications, and workshops on pollinator conservation. Growers. We have given over a dozen joint workshops with Xerces and USDA-NRCS to growers over the last 5 years on pollinator conservation and IPPM. We regularly present at and take a leadership role in the Mid-Atlantic Fruit and Vegetable Convention. The primary audience is growers, along with suppliers and industry. This is the largest convention of fruit and vegetable growers in this part of the US, with decades of successful conferences and attendance of ~1,500 annually. Lopez-Uribe provides both English- and Spanish-language presentations at this conference. Scientific community. Grozinger was invited to participate in the Commission for Environmental Cooperation's North American Pollinator Conservation Workshop (February 2020) and EPA/USDA Pollinator State of the Science Workshop (September 2020). Grozinger served on the Research Oversight Committee for Genome Canada project, "BeeCSI: "omic tools for assessing bee health" (2019-2022), the P-IE Pollinator Committee, Entomological Society of America, 2016-2020, and the co-Chair of the Pollinator Position Statement Writing Group, Entomological Society of America (2019). López-Uribe serves as the vice-president of the American Associationof Professional Apiculturists (AAPA). We served as invited keynote presenters at national and international conferences on bee health (International Conference on Pollinator Biology, Health and Policy, Apimondia, Entomological Society of America, Australian Native Bee Conference). We have hosted numerous national and international researchers on pollinator health for seminars, working group meetings, and visiting researcher programs at Penn State. We have an extensive and active network of international collaborators in Belgium, Canada, China, Germany, Israel, Italy, Kenya, the Netherlands, Spain, Switzerland and the UK. What do you plan to do during the next reporting period to accomplish the goals?We will continue to use the Integrative Pollinator Ecology graduate training program to form closer ties among the faculty involved in this HATCH project and develop novel collaborative research projects.

Impacts
What was accomplished under these goals? Objective 1 (López-Uribe) Evaluating the impact of management practices on honey bee health and productivity. With funding from USDA-OREI we showed honey bee colonies treated with miticides have fewer mites and better winter survival. However, untreated colonies produce significantly more honey and have higher levels of beneficial bacteria in food stores. (Grozinger) National survey of honey bee virus distribution. Screened samples from the 2015 US National Honey Bee Disease Survey for the presence of recently identified viruses. Found twoof the eightnewly identified viruses were broadly distributed, while fourmay represent emerging infections (Ray et al 2020). Project was supported by funding from the USDA-APHIS. (Hines) Epidemiology of pathogens across bee communities in PA. Evaluated pathogen loads in managed and wild bees (funded by NESAREGraduate Research Award and PSU Agricultural College Strategic Networks and Initiatives Program [SNIP]training grant). Found higher levels of Black Queen Cell Virusand Deformed Wing Virusin honey bees than bumble bees, and found bumble bees, unlike honey bees, tend to purge these pathogens over the winter, thus honey bees act as a pathogen reservoir. One bumble bee speciesin particular appears to be especially susceptible to the pathogen Nosema. (Hines, Grozinger) With a USDA FFARgrant we examined the role of landscape factors on bumble bee health. Spring floral resource availability is a leading explanatory factor for bumble bee pathogen loads (McNeil et al., in revision). Secured a USDA-APHIS grant to follow up this study in another region next summer (North Carolina). (López-Uribe) Pathogen dynamics in wild bee populations in agroecosystems. Found fourhoney bee viruses in bumble bees (Bombus impatiens) and squash bees (Eucera P. pruinosa) in pumpkin farms in PA. Detected high prevalence of the eukaryotic pathogens Crithidia spp., Nosema spp. and Apicystis bombi in squash bees. Femalesquash bees generally show higher loads of pathogens than males. Preliminary results suggest these pathogens may be spread through flowers. Funding was from competitive student fellowships from the NSFand NE SARE. (Grozinger, Patch, Hoover)Evaluating the nutritional needs of bees to improve planting schemes. Evaluated the protein and lipid ratios of pollen of 82 plant species and threebee species, and demonstrated a broad range of ratios, which seem to correspond with different preferences for the different bee species (Vaudo et al 2020). Using DNA barcoding, we found in urban landscapes, honey bees foraging preferences shift throughout the growing season from trees, to weedy plants, to ornamental plant species in the fall (Sponsler et al, 2020a, b). We found significant variation in visitation patterns of pollinators to different annual ornamental plant species and cultivars, and found a significant effect of season, year, and site (Erickson et al, 2020). Work was funded by a USDA SCRI grant and a USDA-NIFA-Predoctoral Fellowship. Evaluated the pollinator community visiting flowering black cherry trees in PA forests, to understand how to better support these communities and reverse declines in black cherry regeneration. Work was supported by funding from the PA DCNR and McIntire-Stennis program. (Hines) Evaluating the role of natural floral toxins on wild bees. Examined the role of natural floral toxins in floral visitation bias in bumble bees and the potential for natural tolerance of floral toxins to translate to pesticide tolerance. Strong visitation bias to milkweeds by bumble bee species aligns with lab experiments demonstrating higher levels of tolerance and enhanced ability to detect their toxins in this species. This tolerance did not translate to greater tolerance to neonicotinoid pesticides. Data were used to develop a submitted NSF grant. (Grozinger) Developing a National Insecticide Toxic Load Map. Published a spatial map of pesticide use patterns across the US (Douglas et al 2020). Total toxic load of applied insecticides has increased nationally over the last 20 years, with some counties showing increases of over 100-fold. This map allows stakeholders and policymakers to identify sites to focus alternative management or conservation efforts. Funding was provided by the USDA-NIFA-AFRI, the USDA FFAR, and the National Socio-Environmental Synthesis Center. (Grozinger) Evaluating the role of landscape and climate on wild bee health. To support large-scale studies of the effects of land use, habitat, weather and climate on wild bee species, we organized, validated, and shared an analysis-ready version of one of the few existing long-term monitoring datasets for wild bees in the US (Kammerer et al 2020). Work was supported by funding from the USDA-NIFA Postdoctoral training program and the USDA FFAR. Objective 2 (López-Uribe) Evaluating the genetics of feral (unmanaged) honey bees. With funding from USDA Animal Health program, a USDA FFAR grant, and a PSU College of Agricultural Sciences SNIP graduate training grant, we investigated disease dynamics and immunocompetence in feral and managed honey bee colonies in PA. Colony losses were not significantly different, but the average titers of DWV were higher in feral than in managed colonies (Hinshaw et al in review). With funding from the North American Pollinator Protection Campaign (NAPCC), López-Uribe is working with Brock Harpur from Purdue University on sequencing the genomes of the feral colonies to identify the genetic basis of the viral tolerance phenotypes observed in these colonies. The ultimate goal is to identify traits that can be used in future breeding programs of disease tolerant honey bee lines. (Grozinger) Tools for genetic manipulation of bees. Working with Jason Rasgon (PSU) to develop methods for genetic transformation of bees, which will facilitate the identification and validation of genetic markers for bee health and behavior; project is funded by the NSF-EDGE program. Objective 3 (all faculty members, led by Boyle) PA Pollinator Protection Plan. Worked together with a team of 36 individuals representing 28 state- and national-organizations and stakeholder groups to develop the PA Pollinator Protection Plan (P4). Dr. Natalie Boyle organizes meetings of the P4 group every 4 months. (Grozinger) Beescape. In April 2019, launched an online tool called "Beescape" (beescape.org), which allows users (across the continental US) to explore landscape quality for bees at their selected sites. Using wintering colony survival data from the PA State Beekeepers Association Survey (Calovi et al, in review). Developed a new decision support tool, BeeWinterWise. (López-Uribe and Rajotte) Integrated Pest Management(IPM) is a long standing, science based, decision making process whose ecological roots lie in the use of multiple biological, cultural, physical, and chemical tactics to protect crops in a way that minimizes economic, health, and environmental risks. In an Integrated Pest and Pollinator Management (IPPM) context, both pest management and pollinator protection may be achieved. We have a number of projects in apple, pumpkin and cotton agroecosystems in which we apply this approach. (López-Uribe) Management Practices. Explored the role of management practices in improving health outcomes of honey bee colonies. We demonstrated that variation in management practices among beekeepers is mainly driven by two factors (1) size of the operation and (2) beekeeper's philosophies towards chemical use (Underwood et al 2018). Therefore, there is a clear need for development of best management practices for these different groups of beekeepers. We are comparing the effects of different genetic stocks in collaboration with Purdue University and currently in the process of updating all the factsheets and extension publications related to honey bees and apiculture.

Publications

  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Ghisbain, G., J.D. Lozier, S.R. Rahman, B.D. Ezray, L. Tian, J.M. Ulmer, S. Heraghty, J.P. Strange, P. Rasmont, and H.M. Hines. 2020. Substantial genetic divergence and lack of recent gene flow support cryptic speciation in a color polymorphic bumble bee (Bombus bifarius) species complex. Systematic Entomology, 45 (3):635-652. https://doi.org/10.1111/syen.12419.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Villalona, E., B.D. Ezray, E. Laveaga, A.A. Agrawal, J.G. Ali, and H.M. Hines. 2020. The role of toxic nectar secondary compounds in driving differential bumble bee preferences for milkweed flowers. Oecologia.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: McNeil, D.J., and Grozinger. C.M. Singing in the Suburbs: Point Count Surveys Efficiently Reveal Habitat Associations for Nocturnal Orthoptera Across an Urban-to-Rural Gradient. Journal of Insect Conservation https://doi.org/10.1007/s10841-020-00273-9.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Wu, X., Galbraith, D.A., Jeong, H, Chatterjee, P., C.M Grozinger, and S.V. Yi. Lineage and parent-of-origin effects in DNA methylation of honey bees (Apis mellifera) revealed by reciprocal crosses and whole-genome bisulfite sequencing. Genome Biology and Evolution, evaa133, https://doi.org/10.1093/gbe/evaa133.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Jasper, W.C., Brutscher, L.M., C.M. Grozinger and E.L. Nino. Injection of seminal fluid into the hemocoel of honey bee queens (Apis mellifera) can stimulate post-mating changes. Scientific Reports 10, 11990.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Kammerer, M., Tooker, J.F. and C.M. Grozinger. A long-term dataset on wild bee abundance in Mid-Atlantic United States. Scientific Data 7, 240.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Vaudo, A.D., Tooker, J.F., Patch, H.M., Biddinger, D.J., Coccia, M., Crone, M.K., Fiely, M., Francis, J.S., Hines, H.M., Hodges, M., Jackson, S.W., Michez, D., Mu. J., Russo, L., Safari, M., Treanore, E.D., Vanderplanck, M., Yip, E., Leonard, A.S., C.M. Grozinger. Pollen protein:lipid macronutrient ratios may guide broad patterns of bee species floral preferences. Insects 11(2): 132.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Ray, A.M., Lopez, D.L., Martinez, J.F., Galbraith, D.A., Rose, R., vanEngelsdorp, D., Rosa, C., Evans, J.D., and C.M. Grozinger. Distribution of recently identified bee-infecting viruses in managed honey bee (Apis mellifera) populations in the United States. Apidologie DOI: 10.1007/s13592-020-00757-2.
  • Type: Journal Articles Status: Published 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. Ecosphere 11(4): e03102 DOI: 10.1002/ecs2.3102.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Sponsler, D.B., Grozinger, C.M., Richardson, R., Nurse, A., Brough, D., Patch, H.M., and K. A. Stoner. "A screening-level assessment of the pollinator-attractiveness of ornamental nursery stock using a honey bee foraging assay." Scientific Reports 10(1), 1-9.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Grozinger C.M. and A. Zayed. Genomics for understanding and improving pollinator health in a world of multiple stressors. Nature Reviews Genetics 21: 277291DOI: 10.1038/s41576-020-0216-1.
  • 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: 2020 Citation: Russo, L., Keller, J., Vaudo, A., Grozinger, C.M., K. Shea. Warming increases pollen lipid concentration in an invasive thistle, with minor effects on the associated floral-visitor community. Insects 11(1) 20.
  • Type: Journal Articles Status: Published Year Published: 2020 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 49(1) 178-188.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Vaudo AD, Biddinger DJ, Sickel W, Keller A, L�pez-Uribe MM. (2020) "Phylogenetic pollen preferences facilitate naturalization and pollination services of introduced bees in new habitats." Royal Society Open Science 7(7):200225 doi/10.1098/rsos.200225
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Kilpatrick SK, Gibbs J, Mikulas MM, Spichiger S, Ostiguy N, Biddinger DJ, L�pez-Uribe MM. (2020) "An updated checklist of the bees." (Hymenoptera: Apoidea: Anthophila) of Pennsylvania, United States of America." Journal of Hymenoptera Research https://doi.org/10.3897/jhr.77.49622
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Phan N, Joshi N, Rajotte E, L�pez-Uribe MM, Zhu F, Biddinger DJ. (2020) "A new ingestion bioassay protocol for assessing pesticide toxicity to the adult Japanese orchard bee (Osmia cornifrons)." Scientific Reports. https://doi.org/10.1038/s41598-020-66118-2
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: L�pez-Uribe MM, Ricigliano V, Simone-Finstrom MD (2020) "Defining Pollinator Health: Understanding bee ecological, genetic and physiological factors at the individual, colony and population levels." Annual Review of Animal Bioscience. doi:10.1146/annurev-animal-020518-115045
  • Type: Other 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: Other Status: Published Year Published: 2020 Citation: L�pez-Uribe MM, Biddinger D (2020). "Orchard Pollination: Strategies for Maintaining Pollination Services in Tree Fruit." Pennsylvania State Extension (Newsletter Article) https://extension.psu.edu/orchard-pollination-strategies-for-maintaining-pollination-services-in-tree-fruit
  • Type: Other Status: Published Year Published: 2020 Citation: Grozinger CM, Underwood RM, L�pez-Uribe MM (2019). "Viruses in Honey Bees." Pennsylvania State Extension Pennsylvania State Extension https://extension.psu.edu/viruses-in-honey-bees
  • Type: Other Status: Published Year Published: 2020 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 https://extension.psu.edu/ipm-for-pennsylvania-schools-and-childcares-a-how-to-manual
  • Type: Other Status: Published Year Published: 2020 Citation: Anton, K. and C.M. Grozinger. An Introduction to Queen Honey Bee Development. Penn State Extension. 2020. https://extension.psu.edu/an-introduction-to-queen-honey-bee-development
  • Type: Other Status: Published Year Published: 2020 Citation: Anton, K. and C.M. Grozinger. Queen Cell Production: Grafting and Graft-free Methods. Penn State Extension. 2020. https://extension.psu.edu/queen-cell-production-grafting-and-graft-free-methods
  • Type: Other Status: Published Year Published: 2020 Citation: Anton, K. and C.M. Grozinger. Beekeeping: Cell Builder Basics. Penn State Extension. 2020. https://extension.psu.edu/beekeeping-cell-builder-basics