Source: PENNSYLVANIA STATE UNIVERSITY submitted to
SUSTAINABLE SOLUTIONS TO PROBLEMS AFFECTING BEE HEALTH
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
TERMINATED
Funding Source
Reporting Frequency
Annual
Accession No.
1004871
Grant No.
(N/A)
Project No.
PEN04579
Proposal No.
(N/A)
Multistate No.
NC-_old1173
Program Code
(N/A)
Project Start Date
Nov 28, 2014
Project End Date
Sep 30, 2019
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
Honey bees are essential for pollination of over 90 fruit and vegetable crops worldwide, with the pollination valued at more than $14.6 billion in the U.S. Since 2006, increased colony loss in bee colonies with unique symptoms (termed Colony Collapse Disorder (CCD)) have severely impacted their number and threaten diverse pollination needs of fruit and vegetable producers. In the U.S., the losses due to CCD are combined with major losses due to the parasitic Varroa mite, creating major concern for beekeepers in the U.S. and their economic sustainability. Within the last few years, self-reporting surveys have reveled that approximately 45% of all colonies are lost annually. In addition, other pollinator populations appear to be decreasing, with several species of bumble bees on the verge of extinction. It is essential for both agriculture and natural ecosystems that this be resolved. The honey bee is the primary pollinator of agricultural crops dependent upon insect pollination. Determining how pathogens and pesticides impact bees is needed to ensure healthy ecosystems, dependent upon pollination of flowering plants. CCD has continued to plague the United States, along with increased colony deaths due to other causes. The underlying causes of CCD are complex as revealed by an epidemiological analysis. CCD colonies have high pathogen prevalence, in particular picorna-like viruses; and data indicate that additional stresses such as chemical exposure and lack of adequate nutrition are playing a role. How the interaction among these stresses translates into bee colony loss is still at question. Environmental chemicals may be part of the problem in colony health. Over 70 different pesticides have been found, representing almost all classes of pesticides. How these chemicals interact with each other and affect the bee biology and health is unknown and is of major importance for understanding impacts on colony health and on native pollinators. It is clear that multiple factors are present that impact colonies. How these factors interact and how the combinatorial impacts determine colony health is key to overcoming honey bee colony loss. We propose to analyze the various stress factors and their interactions on colony and pollinator health, asking what mechanisms underlie the increased mortality. We propose to take our findings to create best management practices for the bee keeper, grower, and other stakeholders. This information is essential for our food security and environmental sustainability.
Animal Health Component
0%
Research Effort Categories
Basic
50%
Applied
25%
Developmental
25%
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
2053099107015%
2113099113010%
2163099102010%
3043010108010%
2113010115010%
2113010113015%
2111499116010%
2111199116010%
2111219116010%
Goals / Objectives
To evaluate the role and causative mechanisms of parasitic mites, viruses, and microbes in pollinator abundance and honey bee colony success 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 determine how land management practices affect pollinator nutrition and how nutrition affects honey bee colony productivity and success To assess the effects of exposure to pesticides and other xenobiotics on the survival, health and productivity of honey bee colonies and pollinator abundance and diversity To determine the effects of interactions among various factors affecting pollinator and honey bee colony health To develop and recommend "best practices" for beekeepers, growers, land managers and homeowners to promote honey bee and pollinator health
Project Methods
Objective 1 -- To evaluate the role and causative mechanisms of parasitic mites, viruses, and microbes in pollinator abundance and honey bee colony successColony-level distribution of pathogens: Within colony prevalence and intensity of Nosema ceranae and viral infections will be determined by feeding colonies or caged bees with known doses of pathogens. QT-PCR analysis will be used for determining infection levels of bees with IAPV, DWV, BQCV, SBV and other viral pathogens. Nosema will be determined both from spore counts and QT-PCR. Effects on bees will measured by examining age-specific mortality, colony growth, and measures of bee health (vitellogenin levels, protein concentration, lipid content, and physiological enzyme activities.)Objective 2 -- 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 pathogensAnalysis of diversity: We will use a meta-analysis approach to compare the pedigree relationships of honey bee reproductives (queens and their mates) We will also use microsatellite analysis to compare allelic diversity honey bees. Genetic diversity will also be measured at the molecular level, using genomics. Transcriptomics, microarray analysis and genomic sequencing will be performed in experiments to disect the basis of traits underlying resistance to pathogens and parasites. These data will be linked back to molecular markers to enable stock selection.Objective 3 -- To determine how land management practices affect pollinator nutrition and how nutrition affects honey bee colony productivity and successWe will study how land use and the diversity of foraging resources affect the growth, development, and health of honey bee colonies by experimentally placing hives into landscapes that vary in floral resource quality and diversity, and subsequently measuring variables related to hive health. Analogous studies of how land use and the diversity of foraging resources affect the growth, development, and health of native bees will be done using a commercially available Bombus or Osmia species.The value of specific floral (nutritional) resources for multiple species of wild, native pollinators can be inferred by collecting data on which flower species native pollinators prefer to forage on while collecting pollen and/or nectar. Pollen grains are counted and identified for each pollen load with the goal of determining pollen preferences as well as site-specific bee diversity.Using either the observational or experimental design, the preferred plant species can be determined and this information can be used in land use planning and pollinator restoration work.Objective 4 -- To assess the effects of exposure to pesticides and other xenobiotics on the survival, health and productivity of honey bee colonies and pollinator abundance and diversityAssessing effects of Impacts of co-formulants and their degradates, individually and corporately at sub-lethal levels, on key honey bee behaviors/physiology including memory and learning will be investigated. Toxic or sublethal effects on honey bees of pesticide and inert combinations relative to formulation controls, including interference with associative learning, will be determined by direct feeding or incorporation in artificial nectar or uncontaminated pollen or wax, or by topical application of extracts to bees or brood. Colony-level impacts of formulation ingredients will be determined in field experiments. Frequently found co-formulants in pesticides and spray tank adjuvants will be characterized and their identity confirmed. Hive samples of stored pollen, comb wax, nectar and bees or field floral samples with known or suspected high levels of frequently occurring fungicides, insecticides and other pesticides will be analyzed for active ingredients and inerts on our LCMS-2020 at primarily the > 5 ppb limit of detection (LOD). Portions of priority samples will be preserved and sent to the USDA-AMS-NSL in Gastonia for follow-up residue analysis at a more sensitive 1 ppb LOD. Remaining portions of each sample will be used in toxicity and behavioral studies. After identification of key inert ingredients in agrochemicals used frequently around bees, we will develop an appropriate sensitive method for their analysis, similar to a recent methods developed in our lab for analyzing three trisiloxane surfactants and nonylphenol polyethoxylates. We will use these analytical methods to study the environmental fate of trisiloxane, nonyl- and octylphenol surfactants and other key inerts, including their degradates, in and around beehives. Metabolism of free or formulated inerts and pesticides within bee bioassays (including excreta) or in pollen, wax, nectar and other matrices will be addressed through analysis over time of residues relative to the treatment or dose using the appropriate LC/MS-MS method based on chromatographic, spectral and mass transition comparisons with authentic standards. To assess potential toxicity or other negative impacts of formulation components, inerts alone or in combination with active ingredients will be fed at dose levels detected in hive samples in artificial nectar, royal jelly diet or pollen-substitute cakes to adult bees, queens, drones, and brood, or topically applied, and other factors such as bee behavior and colony longevity evaluated. Mortality and other toxicity symptoms as well as altered behaviors will be scored over the course of the bioassay, and regressed relative to pesticide treatment dosages. Chronic feeding of bioactive formulation ingredients and combinations will also be conducted. Altered behaviors will be investigated further through proboscis extension reflex (PER) bioassays. A tier approach will be used where significant impacts at the larval and adult toxicity bioassay and sublethal PER levels will proceed into semi-field (nuke) or field level studies when priority effects are observed.Field monitoring for pesticide exposure: An important aspect of assessing the effects of pesticides on bees is to identify routes of exposure and measure concentrations of different pesticides to which the bees would be exposed over time. By trapping pollen as it is brought into the hive by honey bees, collecting it on a regular basis and analyzing it for a range of pesticides using liquid chromatography/mass spectrometry, we can monitor exposure by this route over the long term and quantify field realistic levels. We plan to monitor hives in both urban and agricultural environments, and to evaluate toxicity using a Pollen Hazard Quotient (concentration in ppb/LD50 in ug/bee) (Stoner and Eitzer, 2013). 5. To determine the effects of interactions among various factors affecting pollinator and honey bee colony healthObjective 5. To determine the effects of interactions among various factors affecting pollinator and honey bee colony healthMulti-factorial analyses will be done on both experimental manipulations of bees and colonies to evaluate the interactions of various factors and resulting impact on pollinator health, at levels ranging from the molecular, physiological, and colony level. Using these experimental data, field colonies will be measured and evaluated to validate predictions of colony health following exposure to certain factors.Objective 6. To develop and recommend "best practices" for beekeepers, growers, land managers and homeowners to promote honey bee and pollinator healthThe experimental data and findings will be used to develop and recommend the best management practices for stakeholders to promote pollinator health.

Progress 11/28/14 to 09/30/19

Outputs
Target Audience:Our research, extension and education efforts target diverse audiences and communities (see 'How have the results been disseminated to communities of interest?' section). They include members of the public, K-12 and undergraduate students, beekeepers, master gardeners, land managers, growers, industry groups, policymakers, the global scientific community, and non-profit organizations. From January 2018 to October 2018, our outreach and extension efforts reached over 2000 individuals, with nearly 10,000 additional individuals engaged through our efforts at an annual science and agricultural fair (Great Insect Fair and PA Ag Progress Days). Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?Through this project, numerous undergraduate students, graduate students and postdoctoral fellows are being trained. We obtained funding for a graduate training program in Integrative Pollinator Ecology (http://ento.psu.edu/pollinators/graduate-training-program) through funding from the Penn State College of Agricultural Sciences Strategic Initiative Program, the Huck Institutes of the Lifes Sciences and the USDA NNF program. The IPE program will train 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. Together, these programs provide funding for 8 PhD students. Post-doctoral scholars: Kristen Brochu, Nate Pope, Doug Sponsler, Rong Ma, DJ McNeil, Martina Calovi, Li Tian, Colin Wright Graduate students: Melanie Kammerer, Tyler Jones, Emily Erickson, Allyson Ray, Rachel McLaughlin, Makaylee Crone, Sean Bresnahan, Sarah Kania, Briana Ezray, Sarthok Rahman, Chauncy Hinshaw, Shelby Kilpatrick, Brooke Lawrence, Ginamaria Roman-Echvarria, Laura Jones, Stephania Sandoval, Ngoc Phan Undergraduate students: Sheldon Davis, Bryce Buck, Brock Molloy, Cheyenne Dolinsky, Rachel Duke, Matt Poorman, Eris Villalona, Ashley Heimann, Timothy Egner, Margaret Weber, Marena Martinez, Mila Paiva, Ryan Ford 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. The PIs work closely with beekeepers through NE-SARE funded projects on honey bee stock improvement, and our "Tracking Feral Bees" and Beescape Projects. In July 2019, we contributed support (financial and organizational) for the International Conference in Pollinator Health, Biology and Policy, which attracted >200 individuals from academia, industry, government and stakeholder groups. 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. Pennsylvania Pollinator Protection Plan (P4) Task Force and Advisory Board. Grozinger led a team (including Lopez-Uribe and Patch) of 36 individuals, represented 28 national and international organizations, in developing and writing the P4. The P4 is a living document that contains information on the current status and economic value of pollinator in Pennsylvania, best practices for developing foraging and habit, using pesticides, and managing bees in urban, agricultural, and natural landscapes as well as roadsides and rights of way, and recommendations for research, communication, and policy. In total, the document is ~80 pages in length and is extensively hyperlinked. We hosted a meeting of the P4 group at Penn State in November 2018, and hosted a meeting of the PennDOT pollinator working group in April 2019. The P4 is available at http://ento.psu.edu/pollinators/research/the-pennsylvania-pollinator-protection-plan-p4. 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. In addition to outreach to specific groups outlined below, 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 annually at Penn State, and members are invited to present in the Center's Pollinator Health and Policy Seminar Series or attend working group meetings. Outreach to the public. Each year, the Center for Pollinator Research participates in several science fairs, including the Great Insect Fair (Department of Entomology) and PA Ag Progress Days. These events reach >10,000 individuals annually. Outreach to K-12 students. Together with Penn State's Center for Science and the Schools, we received funding from the USDA-PD-STEP program to develop a new program targeting middle- and high-school students from underserved rural and urban communities. We held a workshop from June 24-June28, 2019 at University Park. Instructors: Kathy Hill, Christina Grozinger, Harland Patch, Emily Erickson, Tyler Jones, Doug Sponsler and Melanie Kammerer Allen. This short course provided training for middle and high school teachers to include pollinator research and biology into their classrooms. Additionally, we have created lesson plans and other content that will be available online. Together with faculty in Penn State's Learning, Design and Technology Program (Professor Heather Zimmerman) we developed a 1 hour workshop for families with pre-K through middle school children for use in rural libraries and museums. The workshop was tested in April, July, October 2019. (Instructors: Christina Grozinger, Makaylee Crone, and Rong Ma). Additional activities have been offered by Center members to K-12 students. This included several school visits and presentations about pollinators as part of the PSU "Nature Explorers" summer camp (elementary school) and the Pennsylvania School of Excellence in Agricultural Sciences high school summer program. Education and outreach to 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 also offer annual presentations to Georgia Tech's summer undergraduate research program in urban beekeeping. Extension to 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. Moreover, we recently launched two citizen-scientist project with beekeepers in Pennsylvania and surrounding states: "Tracking Feral Bees" and "Beescape." Extension to 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. Extension to 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 organized one symposia at the International Conference of Pollinator Biology, Policy and Health. Grozinger served on the Research Oversight Committee for Genome Canada/Genome BC project, "Sustaining and Securing Canada's Honey Bees Using 'Omic Tools" (2015-2018), 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. 2015, 2019. 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). 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. Grozinger serves as a PI on a National Socio-Environmental Synthesis Center (SESYNC) Pursuit Program, titled "Putting pesticides on the map to guide conservation of pollinators and their ecosystem services". PIs: Grozinger (PSU), Sponsler (PSU), Douglas (Dickinson), Lonsdorf (U Minn), Thogmartin (USGS). Workshops: November 13-15, 2017, May 30-June 1, 2018, August 12-14, 2019. 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? Goal 1 (Grozinger): Wrote a comprehensive review of bee viral ecology published in Annual Review of Entomology (with M. Flenniken). Building on our previous transcriptomics analyses of the mechanisms mediating host-parasite interactions, we demonstrated that Varroa mite feeding results in increase viral titers due to the removal of hemolymph & associated immune factors. (Hines): We continue to examine the epidemiology of honey & native bee pathogens (viruses, Nosema) across bee communities in central PA. This project addressed how pathogen loads differ between honey & bumble bees, the seasonality of bee pathogens, & the effects of overwintering on pathogen loads by species. This project revealed much higher levels of viruses BQCV & DWV in honey bees than bumble bees, & that bumble bees tend to purge these pathogens over the winter, exhibiting negligible levels in spring queens, whereas honey bees retain these pathogens. These pathogens exhibited seasonal trends that were otherwise similar between these species. Other pathogens, including other viruses & Nosema, occurred at fairly low levels in these communities by comparison. Goal 1 & 5 (Hines): We examined degradation of DWV under a variety of conditions (temp, humidity, floral exp) to assess the duration of its persistence, revealing DWV tends to persist for months in lab settings. We examined whether DWV is directly transmitted between honey bees & the relative mortality, to reveal that bumble bees carry DWV & transmit it to honey bees, which are more susceptible to the pathogen. We have also initiated a project examining relative levels of Nosema, a pathogen considered to be primarily responsible for selective declines among bumble bee species. This project builds on data we collected across PA that one bumble bee in particular (B. perplexus) has unusually high levels & thus may be more a new susceptible species. (Lopez-Uribe): We are investigating pathogen dynamics in wild bee populations in agroecosystems & found the presence of 4 honey bee viruses (DWV, IAPV, KBV, SBPV) in bumble bees (Bombus impatiens) & squash bees (Eucera P. pruinosa) in pumpkin farms in PA. We have also detected high prevalence of eukaryotic pathogens such as Crithidia spp., Nosema spp. & Apicystis bombi in squash bees. Females squash bees generally show higher loads of pathogens than male squash bees. Goal 1 & 2 (Lopez-Uribe): Feral honey bees appear to be more resilient to pathogens & parasites than their managed counterparts. We investigated disease dynamics & immunocompetence in feral & managed honey bee colonies in PA & the role of host-pathogen interactions in overwintering success of honey bees. Colony overwintering losses were recorded at 44% & 42% for managed & feral colonies, respectively for the 17-18 winter & 50% & 59% colony loss for managed & feral colonies, respectively for the 18-19 winter. The average titers of DWV were 2- to 4-fold higher in feral than in managed colonies. We identified several factors that predict overwintering survival in both managed & feral colonies. Specifically, we found that expression of the immune genes Hymenoptaecin & Vago are positively correlated with overwintering success. Goal 3 & 5 (Grozinger): We found that bumble bee foraging preferences are shaped by macronutrient ratios, such that bees preferentially forage for pollen with a specific protein:lipid ratio. We demonstrated that bumble bees will collect the same nutritional quality of food, regardless of the surrounding landscape conditions. The amount of food that they bring in is directly correlated with colony growth & success. We are evaluating whether nutrition influences honey bee foraging preferences by examining pollen collected by honey bees in different landscapes throughout PA, & have found less consistent patterns, suggesting honey bees simply collect the most abundant pollen in the landscape. Using DNA barcoding analysis, we have demonstrated that honey bees preferentially collect pollen from woody plants, with preferences shifting throughout the growing season from trees, to weedy plants, to ornamental plant species in the fall. Thus, planting ornamental plants can extend the forage season for bees. We have evaluated the attraction of diverse pollinators to annual & 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 & cultivars, & found a significant effect of season, year, & site. Goal 3, 4, & 5 (Hines & Grozinger): In the last 2 summers we have examined the role of landscape factors, including habitat quality & pesticide levels, on bumble bee health by examining pathogen levels & levels of immune response in bumble bees, & to some extent honey bees, across sites of varying quality in PA (22 sites in 2018, 41 sites in 2019). Analysis of 2018 data revealed marginally significant associations suggesting sites with high pesticide levels & lower habitat quality harbor higher bumble bee pathogen loads & exhibit greater immune response. Data for 2019 is being analyzed. (Grozinger): Previously, we demonstrated that pollen-based diets significantly improve survival outcomes for bees exposed to pesticides. Makaylee Crone is investigating which component of pollen-based diets (protein or lipids) are most critical. Goals 1, 4, & 5 (Lopez-Uribe & Underwood): We have experimentally tested the effect of miticide treatment on honey bee colony health & productivity. We have demonstrated that honey bee colonies treated with organic & synthetic miticides have fewer mites & better winter survival than those untreated. Untreated colonies produce significantly more honey than treated colonies. The negative impact of miticides on honey production was also demonstrated in a separate study applying oxalic acid to honey bee packages. We have found that the relative abundance of beneficial bacteria such as Lactobacillus kunkeei decreases in bee bread after miticide treatment. Goal 5 (Grozinger, Hines, Lopez-Uribe, & Patch): We launched a new online tool called "Beescape." Beescape provides a tool for beekeepers, gardeners, growers & land managers to assess the quality of their landscapes for supporting managed honey bees & wild bees. It allows a user to select a specific location (i.e. apiary site, garden, farm) & obtain information about the amount of floral resources, overall toxic load of applied insecticides, & the availability of nesting habitat for wild bees in the landscape surrounding the selected location. Users can also see the land use patterns in their area by clicking on the 'crop' icon. We take this public info & distill it into a single, easy-to-use website that everyone can access. Currently, it's available for PA, IN, IL, NY, WV, MI, & WI, but we plan to add additional states as funding permits. Since launching the program, we have had more than 400 beekeepers register with Beescape across the US. Beescape is a partnership of the Center for Pollinator Research at PSU; the USDA-ARS Pasture Systems & Watershed Management Lab; Dickinson College; Purdue Univ; Univ of IL Urbana-Champaign; Univ of MN; Univ of WI; & Univ of CA Davis. It is made possible by funding from USDA-NIFA-AFRI, the Foundation for Food & Agricultural Research, the National Socio-Environmental Synthesis Center, Illinois Specialty Crops Grant & a Penn State Extension Multistate & Integrated Program Grant. We have partnered with Azavea, a Philadelphia based company, to create the Beescape site. Together, we worked with a team of 36 individuals representing 28 state- & national-organizations & stakeholder groups to develop the PA Pollinator Protection Plan (P4).

Publications

  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Ezray, B.D., D.C. Wham, C. Hill, and H.M. Hines. 2019. Unsupervised machine learning reveals mimicry complexes in bumble bees occur along a perceptual continuum. Proceedings of the Royal Society of London, B series, 286: 20191501, https://doi.org/10.1098/rspb.2019.1501.
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Hines, H.M., and S.R. Rahman. 2019. Evolutionary genetics in insect phenotypic radiations: the value of a comparative genomic approach. Current Opinion in Insect Science. 36:90-95. https://doi.org/10.1016/j.cois.2019.08.013
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Wham, D., Ezray, B.D., and H.M. Hines. 2019. Measuring perceptual distance of organismal color pattern using the features of deep neural networks. PREPRINT, bioRxiv, August 15, 2019. https://doi.org/10.1101/736306
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Baker, A., J. Heraty, J. Mottern, J. Zhang, H. M. Hines, A. Lemmon, and E. Lemmon. 2019. Inverse dispersal patterns in a group of ant parasitoids (Hymenoptera: Eucharitidae: Oraseminae) and their ant hosts. Systematic Entomology, https://doi.org/10.1111/syen.12371
  • Type: Other Status: Published Year Published: 2019 Citation: Tian, L., Rahman, S.R., Ezray, B.D., Franzini, L., Strange, J.P., Lhomme, P., and H.M. Hines. 2019. A homeotic shift late in development drive mimetic color variation in a bumble bee. Proceedings of the National Academy of Sciences, USA. 116: 11857-11865. https://doi.org/10.1073/pnas.1900365116
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Dash, S., Rahman, S., Hines, H.M., and W. Feng. 2018. Incremental BLAST: Incremental addition of new sequence databases through e-value correction. PREPRINT, bioRxiv, 476218. https://doi.org/10.1101/476218
  • Type: Conference Papers and Presentations Status: Published Year Published: 2018 Citation: Lhomme, P. and H.M. Hines 2018. Ecology and Evolution of Cuckoo Bumble Bees. Annals of the Entomological Society of America, 112: 122-140.
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: L�pez-Uribe MM, Simone-Finstrom MD (2019) Honey bee research in the US: Current state and solutions to beekeeping problems. Insects 10: 22 doi.org/10.3390/insects10010022
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Cusser S, Grando C, Zucchi MI, L�pez-Uribe MM, Pope NS, Ballare K, Luna-Lucena DC, Neff J, Almeida AEB, Young K, Jha S (2019) Small but critical: semi-natural habitat fragments promote bee abundance in cotton agroecosystems across both Brazil and the United States. Landscape Ecology doi.org/10.1007/s10980-019-00868-x
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Beasley DE, Fitzgerald JL, Fowler A, Keleher K, L�pez-Uribe MM, Dunn RR (2019) Do Bee Wings Adapt for Flight in Urban Environments? Southeastern Naturalist 18(2):183-91
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: L�pez-Uribe MM, Jha S, Soro A. (2019) 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, 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: 2019 Citation: Villar, G., Hefetz, A., and C.M. Grozinger. "Evaluating the Effect of Honey Bee (Apis mellifera) Queen Reproductive State on Pheromone-mediated Interactions with Male Drone Bees" Journal of Chemical Ecology 45(7): 588-597 (2019)
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Treanore, E., Vaudo, A.D., Grozinger, C.M., and S.J. Fleischer. "Examining the nutritional value and effects of different floral resources in pumpkin agroecosystems on Bombus impatiens worker physiology" Apidologie 50(4), 542-552 (2019).
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Ma, R., Rangel, J., and C.M. Grozinger. Honey bee (Apis mellifera) larval pheromones may regulate gene expression related to foraging task specialization BMC Genomics 20(1): 592 (2019).
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Russo, L, Vaudo, A.D., Fisher, C.J., Grozinger, C.M., and K. Shea. Bee community preference for an invasive thistle associated with higher pollen protein content Oecologia 190(4): 901-912 (2019)
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Annoscia, D., Brown, S.P., Di Prisco, G., De Paoli, E., Del Fabbro, S.D., Frizzera, D., Zanni., V., Galbraith, D.A., Caprio, E., Grozinger, C.M., Pennachio, F. and F. Nazzi., "Haemolymph removal by Varroa mite destabilizes the dynamical interaction between immune effectors and virus in bees, as predicted by Volterras model" Proc Roy Soc Bio 286 (1901), 20190331 (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: Flenniken, M.L. and C.M. Grozinger. Bee Viruses: Ecology, Pathogenicity, and Impacts." Annual Review of Entomology 64: 205-226 (2019)
  • Type: Journal Articles Status: Published Year Published: 2019 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 112(2): 525-533 (2019)
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Amsalem, E. and C.M. Grozinger. The importance of holistically evaluating data: a comment on Holman." Behavioral Ecology 29(6), 12101215 (2018)
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Joshi, N. K., T. Leslie, E. Rajotte and D. Biddinger. 2018. Environmental impacts of reduced-risk and conventional pesticide programs differ in commercial apple orchards, but similarly influence pollinator community. Chemosphere. (accepted w/ revisions August 2018)
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Neelendra K. Joshi, Timothy Leslie, Edwin George Rajotte, David Biddinger: Environmental impacts of reduced-risk and conventional pesticide programs differ in commercial apple orchards, but similarly influence pollinator community. Chemosphere 10/2019; 240:1-10.
  • Type: Book Chapters Status: Published Year Published: 2020 Citation: Rittschof, C.R. and C.M. Grozinger. The interplay between cooperation and conflict in the evolution and function of insect societies In: Social Cooperation and Conflict: Biological Mechanisms at the Interface, Walter Wilczynski, Sarah F. Brosnan, eds. Cambridge University Press, Cambridge UK (2020).
  • Type: Other Status: Published Year Published: 2019 Citation: Underwood, R. (2019). Operation Size and Beekeeping Philosophy Influence Management Decisions. The Pennsylvania Beekeeper. February Issue.
  • Type: Other Status: Published Year Published: 2018 Citation: L�pez-Uribe MM, Amon N, Watrous K, Fleischer S. (2018). Who Pollinates Pennsylvania Blueberry Plants? Penn State Extension Fruit Times, May Issue: https://extension.psu.edu/who-pollinates-pennsylvania-blueberry-plants
  • Type: Other Status: Published Year Published: 2018 Citation: L�pez-Uribe MM (2018) Spring bees: Who are they? Where do they live? Penn State Extension Fruit Times. April Issue: https://extension.psu.edu/spring-bees-who-are-they-and-where-do-they-live
  • Type: Other Status: Published Year Published: 2018 Citation: Stivers L, L�pez-Uribe MM (2018). Protecting Pollinators: What Role Can the Greenhouse Industry Play? eGRO alert, 7(7) March Issue: https://e-gro.org/pdf/2018_717.pdf
  • Type: Other Status: Published Year Published: 2018 Citation: Evans KC, L�pez-Uribe MM (2018) Tracking the Health of Feral Bees in Pennsylvania, preliminary results 2017. The Pennsylvania Beekeeper Newsletter. March Issue.


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

Outputs
Target Audience:Our research, extension and education efforts target diverse audiences and communities (see 'How have the results been disseminated to communities of interest?' section). The include members of the public, K-12 and undergraduate students, beekeepers, master gardeners, land managers, growers, industry groups, policymakers, the global scientific community, and non-profit organizations. From January 2018 to October 2018, our outreach and extension efforts reached over 2000 individuals, with nearly 10,000 additional individuals engaged through our efforts at an annual science and agricultural fair (Great Insect Fair and PA Ag Progress Days). Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?We recently received funding for a graduate training program in Integrative Pollinator Ecology (http://ento.psu.edu/pollinators/graduate-training-program) through funding from the Penn State College of Agricultural Sciences Strategic Initiative Program, the Huck Institutes of the Lifes Sciences and the USDA NNF program. The IPE program will train 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. Together, these programs provide funding for 8 PhD students. Through this HATCH project, numerous undergraduate students, graduate students and postdoctoral fellows are being trained. 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. Pennsylvania Pollinator Protection Plan (P4) Task Force and Advisory Board. Grozinger led a team (including Lopez-Uribe and Patch) of 36 individuals, represented 28 national and international organizations, in developing and writing the P4. The P4 is a living document that contains information on the current status and economic value of pollinator in Pennsylvania, best practices for developing foraging and habit, using pesticides, and managing bees in urban, agricultural, and natural landscapes as well as roadsides and rights of way, and recommendaitons for research, communication, and policy. In total, the document is ~80 pages in length and is extensively hyperlinked. It is available at http://ento.psu.edu/pollinators/research/the-pennsylvania-pollinator-protection-plan-p4. Stakeholder Groups. In addition to outreach to specific groups outlined below, 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 annually at Penn State, and members are invited to present in the Center's Pollinator Health and Policy Seminar Series or attend working group meetings. Outreach to the public. Each year, the Center for Pollinator Research participates in several science fairs, including the Great Insect Fair (Department of Entomology) and PA Ag Progress Days. These events reach >10,000 individuals annually. Outreach to K-12 students. Together with Annmarie Ward, Director of Penn State's Center for Science and the Schools, we received funding from the USDA-PD-STEP program to develop a new program targeting middle- and high-school students from underserved rural and urban communities. We held a workshop from July 24-July 28, 2017 and April 13, 2018 at University Park. Instructors: Annmarie Ward, Christina Grozinger, Harland Patch, Kathy Hill, Emily Erickson, Tyler Jones and Doug Sponsler. This short course provided training for middle and highschool teachers to include pollinator research and biology into their classrooms. Additional activities have been offered by Center members to K-12 students. The included school visits, a one-week "Bug Camp" offered by the PSU Department of Entomology which included activities from program faculty. We also team-taught a summer-long Upward Bound program for first-generation high school students that teaches the life sciences through pollinators (Coordinators: Briana Ezray, Heather Hines). Education and outreach to undergraduate students. We work with Penn State's undergraduate Beekeeping Club, and support student training in 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 also offer annual presentations to Georgia Tech's summer undergraduate research program in urban beekeeping. Extension to 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. Moreover, we recently launched two citizen-scientist project with beekeepers in Pennsylvania and surrounding states: "Tracking Feral Bees" and "Landscapes for Bees". Extension to 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. 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. Extension to 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 co-organized two symposia at the International Conference of Entomology (September 2017) which featured presentations from several members of groups. We served as invited keynote presenters at international conferences on bee health in Romania and Kenya. We have hosted numerous national and international researchers on pollinator health for seminars, working group meeting, 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. Grozinger serves as a PI on a National Socio-Environmental Synthesis Center (SESYNC) Pursuit Program, titled "Putting pesticides on the map to guide conservation of pollinators and their ecosystem services". PIs: Grozinger (PSU), Sponsler (PSU), Douglas (Dickinson), Lonsdorf (U Minn), Thogmartin (USGS). Publications: Sponsler, D.B., Grozinger, C.M., Hitaj, C., Rundlöf, M., Botías, 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 (submitted). Workshops: November 13-15, 2017, May 30-June 1, 2018, January 8-10, 2019. What do you plan to do during the next reporting period to accomplish the goals?We plan to using the new 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? We have conducted multiple transcriptomics analyses of the mechanisms mediating host-parasite interactions, including leading an international consortium in performing a meta-analysis of 19 transcriptomic studies to identify suites of genes that are commonly & uniquely regulated in response to Nosema, Varroa and viral infections. We conducted studies to identify transcriptional biomarkers of honey bee colony collapse. We are also using meta-genomic approaches to survey global pollinator populations for undiscovered viruses in a project funded by USDA-APHIS, & have identified several novel viruses. Additionally, we have screened samples of bees collected in the 2015 US Nat'l Honey Bee Disease Survey (in collaboration with Jay Evans at USDA-ARS, a total of 809 apiaries were from 36 states were included in this survey) & found that 2 of the 8 newly identified viruses were broadly distributed across the US. We have explored the role of management practices in improving health outcomes of honey bee colonies. We evaluated the impact of different methods for oxalic acid treatment on hives, & published a manuscript in a key trade journal. In Kenya, we evaluated the effect of using different hive types of hive occupation, disease levels, & absconding rates & found that the primary factor determining these parameters was the duration of time since colony founding & colony size. Thus, we recommend beekeepers use the hive types that are most economical & efficient for their operations, but also allow periodic absconding & swarming. Feral (unmanaged) honey bees appear to be more resilient to pathogens & parasites then their managed counterparts. We are examining the role of genetics & enviro (management) on this resilience. We demonstrated that higher immunocompetence in feral bees is associated with higher genetic diversity & received funding from USDA Animal Health program to compare disease levels & immunocompetence in feral & managed honey bee colonies in Pa, using a citizen-science approach. Additionally, we completed a series of experiments evaluating the role of genetics in overwintering survival & found, for the stocks that we analyzed, there was no impact of genetic background, & location of the apiary was the main determinant of survival. We are working with Jason Rasgon (PSU) to develop methods for genetic transformation of bees, which will facilitate the identification & validation of genetic markers for bee health and behavior; this project was funded by a grant USDA Exploratory Res program, the USDA Postdoc Fellows program, & 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. We are examining the impact of nutrition & rearing conditions on various metrics of bumble bee health. This project is near completion & has revealed that pollen nutrition has the largest effect on bee health & bee coloration although climate plays a role, & that bee coloration is a potential bioindicator of the nutritional quality available to bees in natural landscapes. Additional projects are examining the genetic basis for colour pattern variation between species & populations of bumble bees, & how colour patterns are controlled by developmental processes. Finally, we have estimated the surprisingly large diversity bees in agroecosystems, evaluated the role of landscape in shaping pollinator communities & influencing pollination services in agroecosystems, & created pollinator habitat and assessed its impacts on bee communities & pollination services. We have developed a spatial map of pesticide use patterns across the US, by incorporating data from the USDA Crop Land, Census of Ag, NASS survey database, USGS Pesticide Nat'l Synthesis Project, & EPA Ecotox Database. This map will allow us to evaluate spatial & temporal trends in pesticide use patterns & potential toxicity to bees. We have launched a new program called "Landscapes for Bees", in which we obtain data on colony health metrics & management infor from beekeepers in Pa and surrounding states & determine how these correlate with generalizable indices of features in the landscape, including forage resource quality & pesticide exposure risk. Preliminary data & analyses found a strong correlation between survival & Varroa management, forage quality, pesticide use, & honey bee colony density. These studies are in collaboration with Eric Lonsdorf (Univ of Minnesota) & the USDA-ERS, & are partially funded by a grant from the North American Pollinator Protection Campaign. We worked together with a team of 36 individual representing 28 state-and national-organizations and stakeholder groups to develop the Pa Pollinator Protection Plan (P4). It summarizes the current state of pollinators in Pa, & provides recommendations for best practices & resources to support & expand pollinator populations. 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, & chemical tactics to protect crops in a way that minimizes economic, health, & environmental risks. IPM can address any pest complex (insect, disease, weed, vertebrate, etc.) & can be adapted to any ag production goals including conventional, sustainable & organic. IPM can be adjusted to protect pollinator health just as it is adjusted to protect other beneficial organisms such as predators & parasitoids. In an Integrated Pest & Pollinator Management (IPPM) context, both pest management & pollinator protection may be achieved. We have a number of projects in apple, pumpkin & cotton agroecosystems in which we apply this approach. We evaluated the impact of different methods for oxalic acid treatment on hives, & published a manuscript in a key trade journal. A review & recommendations for IPM approaches for managing Nosema microsporian populations in honey bee hives was published in the Journal of Economic Entomology. Additionally, we are examining the epidemiology of bee pathogens in insect communities. In this large-scale project we are screening bee communities in sites across central Pa 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 & between bee & 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 this data will allow us to build a model for pathogen spread and provide a holistic understanding of how pathogens can impact communities. The bees & pollen for this project have been collected & we are in the middle of pathogen screening. Grad student Briana Ezray is leading this project & has secured a NE SARE Grad Res Award & North American Pollinator Protection Campaign grant to fund the proposed goals. Finally, we are investigating (1) the population demography & pathogen pressures of native populations, and (2) the consequences of the evolution of sociality for immune systems in bees. The two major accomplishments include: The detailed reconstruction of the evolutionary history of the squash bee, an important native pollinator for crop production, and (2) evidence showing that social bee species have lower cellular immune responses than solitary species, which may have important implications for how bee species with different levels of sociality respond to pathogen pressures.

Publications

  • Type: Journal Articles Status: Under Review Year Published: 2018 Citation: Miko, I., S.R. Rahman, S. Anzaldo, T. van de Kamp, B.A. Parslow, N.J. Tatarnic, M.T. Wetherington, J. Anderson, R.J. Schilder, J.M. Ulmer, A.R. Deans, and H.M. Hines. Fat in the leg: function of the expanded hind leg in gastruptiid wasps. Insect Systematics and Diversity
  • Type: Other Status: Under Review Year Published: 2018 Citation: Tian, L. and H.M. Hines. Morphological characterization and staging of bumble bee pupae. PeerJ
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Lhomme, P. and H.M. Hines. 2018. Ecology and evolution of cuckoo bumble bees. Annals of the Entomological Society of America, https://doi.org/10.1093/aesa/say031
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Lhomme, P. and H.M. Hines. 2018. Reproductive dominance strategies in insect social parasites. Journal of Chemical Ecology, https://doi.org/10.1007/s10886-018-0971-z
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Harpur, B.A., A. Dey, J.R. Albert, S. Patel, H.M. Hines, M. Hasselmann, L. Packer, and A. Zayed. 2017. Queens and workers contribute differently to adaptive evolution in bumble bees and honey bees. Genome Biology and Evolution 9(9): 2395-2403
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Hines, H.M., P. Witkowski, J.S. Wilson, K. Wakamatsu. 2017. Melanic variation underlies aposematic color variation in two hymenopteran mimicry systems. PLOS ONE 12(7): e0182135
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Brasero, N., Martinet, B., Lecocq, T., Lhomme, P., Biella, P., Valterov�, I., Urbanov�, K., Cornalba, M., Hines, H. (Author), & Rasmont, P. (2017). The cephalic labial gland secretions of two socially parasitic bumblebees Bombus hyperboreus (Alpinobombus) and Bombus inexspectatus (Thoracobombus) question their inquiline strategy. Insect Science. ISBN/ISSN #/Case #/DOI #: 10.1111/1744-7917.12408
  • 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): 1-14 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, Mathews S, L�pez-Uribe MM, Dunn RR, Smith AA (2018) External immunity in ant societies: sociality and colony size do not predict investment in antimicrobials. Royal Society Open Access. DOI: 10.1098/rsos.171332
  • 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
  • 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: 2018 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: 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: 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: 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: 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: 2018 Citation: Mia G. Park, Neelendra K. Joshi, Edwin G. Rajotte, David J. Biddinger, John E. Losey, Bryan N. Danforth: Apple grower pollination practices and perceptions of alternative pollinators in New York and Pennsylvania. Renewable Agriculture and Food Systems 04/2018;, DOI:10.1017/S1742170518000145
  • Type: Journal Articles Status: Accepted Year Published: 2018 Citation: Shugrue, S., Joshi, N. K., Leslie, T., Rajotte, E., and D. Biddinger. 2018. Diversified floral resource plantings support bee communities after apple bloom in commercial orchards. Nature Scientific Reports. (accepted w/ minor revisions May 2018).
  • Type: Journal Articles Status: Accepted Year Published: 2018 Citation: Joshi, N. K., T. Leslie, E. Rajotte and D. Biddinger. 2018. Environmental impacts of reduced-risk and conventional pesticide programs differ in commercial apple orchards, but similarly influence pollinator community. Chemosphere. (accepted w/ revisions August 2018).
  • Type: Journal Articles Status: Published 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). Florida Entomologist, 100(4):809-812.
  • 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: Other Status: Published Year Published: 2018 Citation: L�pez-Uribe MM, Amon N, Watrous K, Fleischer S. (2018). Who Pollinates Pennsylvania Blueberry Plants? Penn State Extension Fruit Times, May Issue: https://extension.psu.edu/who-pollinates-pennsylvania-blueberry-plants
  • Type: Other Status: Published Year Published: 2018 Citation: L�pez-Uribe MM (2018) Spring bees: Who are they? Where to they live? Penn State Extension Fruit Times. April Issue: https://extension.psu.edu/spring-bees-who-are-they-and-where-do-they-live
  • Type: Other Status: Published Year Published: 2018 Citation: Stivers L, L�pez-Uribe MM (2018). Protecting Pollinators: What Role Can the Greenhouse Industry Play? eGRO alert, 7(7) March Issue: https://e-gro.org/pdf/2018_717.pdf
  • Type: Other Status: Published Year Published: 2018 Citation: Evans KC, L�pez-Uribe MM (2018) Tracking the Health of Feral Bees in Pennsylvania, preliminary results 2017. The Pennsylvania Beekeeper Newsletter. March Issue.
  • Type: Other Status: Published Year Published: 2017 Citation: L�pez-Uribe MM (2017) Tracking the health of feral honey bees in Pennsylvania. Penn State Extension Fruit Times. September Issue: https://extension.psu.edu/tracking-the-health-of-feral-honey-bees-in-pennsylvania
  • Type: Other Status: Published Year Published: 2017 Citation: L�pez-Uribe MM (2017) Why are bees the best pollinators? The Pennsylvania Beekeeper Newsletter. October Issue.


Progress 10/01/16 to 09/30/17

Outputs
Target Audience:Our research, extension and education efforts target diverse audiences and communities (see 'How have the results been disseminated to communities of interest?' section). The include members of the public, K-12 and undergraduate students, beekeepers, master gardeners, land managers, growers, industry groups, policymakers, the global scientific community, and non-profit organizations. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?We recently received funding for a graduate training program in Integrative Pollinator Ecology (http://ento.psu.edu/pollinators/graduate-training-program) through funding from the Penn State College of Agricultural Sciences Strategic Initiative Program, the Huck Institutes of the Lifes Sciences and the USDA NNF program. The IPE program will train 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. Together, these programs provide funding for 8 PhD students. Through this HATCH project, numerous undergraduate students, graduate students and postdoctoral fellows are being trained. Post-doctoral scholars: Carolina Grando, Anthony Vaudo, David Galbraith, Maggie Douglas, Doug Sponsler, Rong Ma, Li Tian, Patrick Lhomme. Graduate students: Gabriel Villar, Mehmet Doke, Melanie Kammerer, Tyler Jones, Emily Erickson, Ryan Reynolds, Julia Fine, Saundra Wheeler, Courtnee Eddington, Briana Ezray, Sarthok Raman, Chauncy Hinshaw and Shelby Kilpatrick. Undergraduate students: Dalton Brough, Rachel Kaneshiki, Katelin Quanbeck, Mengyu Liu, McKenzie Schade, Daniel Snellings, Sarah Williams, Anna Nixon, Carrie Hill, Casey Carr, Timothy Egner 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 and the general education course ENT 202 "The Insect Connection", which is taught both semesters and online, and thus reaches hundreds of students annually. The PIs work closely with beekeepers through NE-SARE funded projects on honey bee stock improvement, and our newly launched "Tracking Feral Bees" and "Landscapes for Bees" project. In May 2017 we hosted the Annual Center for Pollinator Research Symposium which attracted ~50 individuals from the Center and representatives of government and stakeholder groups. 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. Stakeholder Groups. In addition to outreach to specific groups outlined below, 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 annually at Penn State, and members are invited to present in the Center's Pollinator Health and Policy Seminar Series or attend working group meetings. Outreach to the public. Each year, the Center for Pollinator Research participates in several science fairs, including the Great Insect Fair (Department of Entomology), Wings in the Park (Penn State Master Gardeners), and Exploration U (Eberly College of Science), and Garden Days at the Arboretum at Penn State. These events reach >5000 individuals annually. Outreach to K-12 students. Together with Annmarie Ward, Director of Penn State's Center for Science and the Schools, we recently received funding from the USDA-PD-STEP program to develop a new program targeting middle- and high-school students from underserved rural and urban communities. We hosted a one-week workshop in July 2017 that trained 17 teachers. Education and outreach to undergraduate students. We work with Penn State's undergraduate Beekeeping Club, and support student training in 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 and the general education course ENT 202 "The Insect Connection", which is taught both semesters and online, and thus reaches hundreds of students annually. Extension to 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. Moreover, we recently launched two citizen-scientist project with beekeepers in Pennsylvania and surrounding states: "Tracking Feral Bees" and "Landscapes for Bees". Extension to 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. 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. Extension to 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 largestconvention 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 co-organized two symposia at the International Conference of Entomology (September 2017) which featured presentations from several members of groups. We served as invited keynote presenters at international conferences on bee health in Romania and Kenya. We have hosted numerous national and international researchers on pollinator health for seminars, working group meeting, 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 plan to using the new 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? We have conducted multiple transcriptomics analyses of the mechanisms mediating host-parasite interactions, including leading an international consortium in performing a meta-analysis of 19 transcriptomic studies to identify suites of genes that are commonly and uniquely regulated in response to Nosema, Varroa and viral infections. We are also using meta-genomic approaches to survey global pollinator populations for undiscovered viruses, and have identified several novel viruses. In this large-scale project we are screening bee communities in sites across central Pa for a panel of known bee pathogens to address the following questions: Do pathogens have different prevalence in bees that differ in sociality and community interactions? How are pathogens circulated within & between bee & non-bee species? How are pathogens within these bees predicted by the community of pathogens present on flowers? Is there a seasonality to pathogen prevalence? How do pathogens flow across the landscape? We have explored the role of management practices in improving health outcomes of honey bee colonies. We evaluated the impact of different methods for oxalic acid treatment on hives, and published a manuscript in a key trade journal. In Kenya, we evaluated the effect of using different hive types of hive occupation, disease levels, & absconding rates & found that the primary factor determining these parameters was the duration of time since colony founding and colony size. Thus, we recommend beekeepers use the hive types that are most economical & efficient for their operations, but also allow periodic absconding and swarming. Feral honey bees appear to be more resilient to pathogens and parasites then their managed counterparts. We are examining the role of genetics & environment on this resilence. We demonstrated that higher immunocompetence in feral bees is associated with higher genetic diversity. Compare disease levels & immunocompetence in feral & managed honey bee colonies in Pa, using a citizen-science approach. Additionally, we completed a series of experiments evaluating the role of genetics in overwintering survival & found, for the stocks that we analyzed, there was no impact of genetic background, and location of the apiary was the main determinant of survival. With collaborators at USDA-ARS, we have identified genes in key honey bee parasites which could serve as excellent targets for RNAi approaches & used these approaches to reduce microsporidian populations in honey bees. We demonstrated that paternally & maternally inherited alleles can significantly influence honey bee physiology & behavior, and thus this information should be taken into consideration when designing crosses. Our research has led to new models in pollinator nutritional ecology. We demonstrated that bumble bee foraging preferences are shaped by macronutrient ratios, such that bees preferentially foraging for pollen with a specific protein:lipid ratio. We are currently working with Ernst Conservation Seeds to screen stocks of native flowering plants to identify those that will optimally support bee nutritional needs, allowing us to designed targeted planting recommendations for agricultural lands or habitat restoration projects. We are examining the impact of nutrition and rearing conditions on various metrics of bumble bee health. This project has revealed that pollen nutrition has the largest effect on bee health & 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. With collaborators from Italy, we demonstrated that the lipid fraction of pollen plays a critical role in the resilience of honey bees to Varroa and viruses.We have estimated the surprisingly large diversity bees in agroecosystems, evaluated the role of landscape in shaping pollinator communities & influencing pollination services in agroecosystems, & created pollinator habitat and assessed its impacts on bee communities & pollination services. Honey bees are sensitive to widespread co-formulants used in agrochemicals, and evaluation of the role of these 'inerts or inactives' in pollinator decline is only in its formative stages. Effects include learning impairment for adult bees and oral toxicity for larvae and adults. Adjuvants and co-formulants generally greatly enhance the pesticidal efficacy and inadvertently the non-target effects of the active ingredient. Organosilicone surfactants are the most potent tank adjuvants & super-penetrants available to growers. Based on the CA Dept of Pesticide Regulation data for agrochemical applications to almonds, there has been increasing use of adjuvants, particularly organosilicone surfactants, during bloom when two-thirds of US honey bee colonies are present. Increased tank-mixing of these with fungicides & insect growth regulators may be associated with recent US honey bee declines. Spray tank adjuvants are largely assumed to be biologically inert & are not registered by the US-EPA. Formulation composition & not just the dose of active ingredient makes the poison.We have found adjuvants like organosiloxane, nonylphenol & octylphenol polyethoxylate surfactants & the co-solvent N-methyl-2-pyrrolidone (NMP) at ppm levels in beehive samples. We found adjuvants like organosilicone surfactants or the solvent NMP alone are orally and topically toxic to bees. We found an organosilicone surfactant adjuvant frequently used during almond pollination, when combined at a field-relevant concentration with prevalent bee viruses, causes synergistic mortality in honey bee larvae. We demonstrated that formulations are generally more toxic than respective active ingredients, particularly fungicides, by up to 26,000-fold. We have found 100% of co-formulants analyzed for in beehive samples, while only 70% of pesticide active ingredients searched for have been detected. We have launched a new program called "Landscapes for Bees", in which we obtain data on colony health metrics and management information from beekeepers in Pa & surrounding states and determine how these correlate with generalizable indices of features in the landscape, including forage resource quality and pesticide exposure risk. Preliminary data & analyses found a strong correlation between survival & Varroa management, forage quality, pesticide use, and honey bee colony density. We worked together with a team of 36 individual representing 28 state-and national-organizations and stakeholder groups to develop the Pa Pollinator Protection Plan (P4): It summarizes the current state of pollinators in Pa, and provides recommendations for best practices & resources to support & expand pollinator populations. The P4 focuses on best practices for forage and habitat, pesticide use, and beekeeping in urban, agricultural, natural & 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 & can be adapted to any ag 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 & pollinator protection may be achieved. We have a number of projects in apple, pumpkin & cotton agroecosystems in which we apply this approach. We evaluated the impact of different methods for oxalic acid treatment on hives.

Publications

  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Van Belleghem, S., Rastas, P., Papanicolaou, A., Martin, S., Arias, C., Supple, M., Hanly, J., Mallet, J., Lewis, J., Hines, H., Ruiz, M., Salazar, C., Linares, M., Moreira, G., Jiggins, C., Counterman, B., McMillan, W. Owen, & Papa, R. (2017). Complex modular architecture around a simple toolkit of wing pattern genes. Nature Ecology & Evolution. ISBN/ISSN #/Case #/DOI #: 10.1038/s41559-016-0052
  • Type: Journal Articles Status: Accepted Year Published: 2017 Citation: Dorchin A, L�pez-Uribe MM, Praz CJ, Griswold T, Danforth BN (Accepted) Phylogeny and new generic-level classification of the Eucera complex (Hymenoptera: Apidae: Eucerini partim). Molecular Phylogenetics and Evolution.
  • Type: Other Status: Other Year Published: 2017 Citation: Hamblin AL�, Youngsteadt E, L�pez-Uribe MM, Frank SD. (2017) Physiological thermal limits predict differential responses of bees to urban heat-island effects. Biology Letters
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: L�pez-Uribe MM, Fitzgerald AM�, Simone-Finstrom MD. (2017) Glucose oxidase production after colony infection: Testing its role in honey bee social immunity. Royal Society Open Science 4:170224. doi: 10.1098/rsos.170224
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: L�pez-Uribe MM, Soro A, Jha S (2017). Conservation genetics of bees: Advances in the application of molecular tools to guide bee pollinator conservation. Conservation Genetics 18:501-506. doi: 10.1007/s10592-017-0975-1
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: L�pez-Uribe MM, Appler RH, Youngsteadt E, 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: 10.1007/s10592-017-0942-x
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Kammerer, M. A., D. J. Biddinger, E. G. Rajotte, and D. Mortensen. 2016. Local plant diversity across multiple habitats supports a diverse wild bee community in Pennsylvania apple orchards. Environ. Ent. 45(1):32-38.
  • Type: Journal Articles Status: Published 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: 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: 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: 2016 Citation: Vaudo, A.D., Stabler D., Patch, H.M., Tooker, J.F., Grozinger, C.M., Wright, G.A. "Bumble bees regulate their intake of the essential protein and lipid pollen macronutrients" Journal of Experimental Biology 219: 3962-3970 (2016)
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Galbraith, D.A., Yi, S.V., and C.M. Grozinger. "Evaluation of possible proximate mechanisms underlying the kinship theory of intragenomic conflict in social insects" Integrative and Comparative Biology 56 (6): 1206-1214 (2016)
  • Type: Other Status: Published Year Published: 2017 Citation: L�pez-Uribe MM. (2017) Oxalic Acid: Why, When, and How? The Pennsylvania BeekeeperNewsletter. July Issue
  • Type: Other Status: Published Year Published: 2017 Citation: Evans KC, Ostiguy N, L�pez-Uribe MM. (2017) Efficacy of different methods of oxalic acid application. American Bee Journal 157:505-507.
  • Type: Other Status: Published Year Published: 2017 Citation: L�pez-Uribe MM. (2017) Tracking the Health of Feral Bees in Pennsylvania. The Pennsylvania Beekeeper Newsletter. February Issue:


Progress 10/01/15 to 09/30/16

Outputs
Target Audience:Our research, extension and education efforts target diverse audiences and communities (see 'How have the results been disseminated to communities of interest?' section). The include members of the public, K-12 and undergraduate students, beekeepers, master gardeners, land managers, growers, industry groups, policymakers, the global scientific community, and non-profit organizations. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?Through this project, numerous undergraduate students, graduate students and postdocs are being trained. Post-doctoral scholars: Jing Chen, David Galbraith, Claire Rittschof, Etya Amsalem, Li Tian, Patrick Lhomme. Graduate students: Gabriel Villar, Anthony Vaudo, Mehmet Doke, Tyler Jones, Emily Erickson, Ryan Reynolds, Julia Fine, Saundra Wheeler, Courtnee Eddington, Briana Ezray, Sarthok Raman. Undergraduate students: Daniel Snellings, Paige Witkowski, Sarah Williams, Anna Nixon, Carrie Hill, Jesse Schneider, Gracy Billy, Tim Groh, Christina Dietz, Sarah McTish. Furthermore, the PIs have collaborated with other research groups to train additional graduate students (Erin Treanore, Carley Miller, Zach Fuller, Melanie Kammerer) and postdoctoral researchers (Vanessa Vacias). 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 and the general education course ENT 202 "The Insect Connection", which is taught both semesters and online, and thus reaches hundreds of students annually. The PIs work closely with beekeepers through NE-SARE funded projects on honey bee stock improvement, and our newly launched "Landscapes for Bees" project. In July 2016, we hosted the 3rd International Conference on Pollinator Biology, Health and Policy. It was attended by 235 individuals from 14 countries, and featured 45 talks and 86 posters. This is the premiere pollination ecology conference in the world, and is attended by individuals in academia, government agencies, nonprofit groups, stakeholder groups and industry groups. This provided an excellent opportunity for students and postdoctoral researchers to present their work and network with the global pollinator community. 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. Stakeholder Groups. In addition to outreach to specific groups outlined below, 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 annually at Penn State, and members are invited to present in the Center's Pollinator Health and Policy Seminar Series or attend working group meetings. Outreach to the public. Each year, the Center for Pollinator Research participates in several science fairs, including the Great Insect Fair (Department of Entomology), Wings in the Park (Penn State Master Gardeners), and Exploration U (Eberly College of Science). These events reach >5000 individuals annually. Outreach to K-12 students. Each year, the Center for Pollinator Research participates in the Arbor and Earth Days celebration at the Arboretum at Penn State. During this event, 600 fourth graders participate in activities related to ecology and conservation. Together with Annmarie Ward, Director of Penn State's Center for Science and the Schools, we recently received funding from the USDA-PD-STEP program to develop a new program targeting middle- and high-school students from underserved rural and urban communities. Education and outreach to undergraduate students. We work with Penn State's undergraduate Beekeeping Club, and support student training in 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 and the general education course ENT 202 "The Insect Connection", which is taught both semesters and online, and thus reaches hundreds of students annually. Extension to beekeepers. Members of the Center for Pollinator Research regularly present at and play a leadership role in local, regional and national beekeeper conferences, and students from the CPR have received awards from several of these organizations. Moreover, we recently launched a citizen-scientist project with beekeepers in Pennsylvania and surrounding states called "Landscapes for Bees". Extension to gardeners and land managers. Members of the Center for Pollinator Research have worked 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. 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. Extension to 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. Center for Pollinator Research members 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 largestconvention of fruit and vegetable growers in this part of the US, with decades of successful conferences and attendance of ~1,500 annually. Scientific community. In addition to individual publications resulting from our programs, Grozinger also co-edited a special issue of Current Opinion in Insect Science which featured review articles from Grozinger, Patch, Biddinger, Mullin, Rajotte and their students. Grozinger co-organized two symposia at the International Conference of Entomology which featured presentations from several members of groups. As noted above, we hosted the 3rd International Conference on Pollinator Biology, Health and Policy in July 2016, and work from our group was presented in both oral and poster presentations. The PIs 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?In addition to the planned research projects, which are exploring multiple questions and research directions, we have submitted proposals for funding a graduate training program in applied integrative pollinator ecology. Such a program would allow us to better integrate the research expertise from across our group and incorporate additional faculty from the Center for Pollinator Research.

Impacts
What was accomplished under these goals? We have conducted multiple transcriptomics analyses of the mechanisms mediating host-parasite interactions, including leading an international consortium in performing a meta-analysis of 19 transcriptomic studies to identify suites of genes that are commonly and uniquely regulated in response to Nosema, Varroa and viral infections.We are also using meta-genomic approaches to survey global pollinator populations for undiscovered viruses in a project funded by USDA-APHIS, and have identified at least seven novel virus.The bees and pollen for this project have been collected and we are in the middle of pathogen screening.Finally, we are investigating (1 the population demography and pathogen pressures of native populations, and (2 the consequences of the evolution of sociality for immune systems in bees.The two major accomplishments include:The detailed reconstruction of the evolutionary history of the squash bee, an important native pollinator for crop production, and evidence showing that social bee species have lower cellular immune responses than solitary species, which may have important implications for how bee species with different levels of sociality respond to pathogen pressures.We have identified genes in key honey bee parasites which could serve as excellent targets for RNAi approaches and used these approaches to reduce microsporidian populations in honey bees.Additionally, we are working with Jason Rasgon to develop methods for genetic transformation of bees, which will facilitate the identification and validation of genetic markers for bee health and behavior.We demonstrated that paternally and maternally inherited alleles can significantly influence honey bee physiology and behavior, and thus this information should be taken into consideration when designing crosses.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.Finally, we have investigated the pheromonal communication systems between drones and queens, and demonstrated that components of mated queen pheromone blend (versus virgin queen blends) appear to repel drones during mating flights, drones secrete compounds which support the formation of drone congregation areas during mating flights, and queen pheromone influences the rates of sexual maturation of drones.This information may allow beekeepers to better control the timing of sexual maturation of drones and queens in breeding operations.Our research has led to new models in pollinator nutritional ecology.We demonstrated that bumble bee foraging preferences are shaped by macronutrient ratios, such that bees preferentially foraging for pollen with a specific protein:lipid ratio.We are currently working with Ernst Conservation Seeds to screen stocks of native flowering plants to identify those that will optimally support bee nutritional needs, allowing us to designed targeted planting recommendations for agricultural lands or habitat restoration projects.This approach has been incorporated into the research plans of recent USDA-SCRI grant to identify ornamental plant stocks that best support pollinator populations.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.Additional projects are examining the genetic basis for colour pattern variation between species and populations of bumble bees, and how colour patterns are controlled by developmental processes.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.Honey bees are sensitive to widespread co-formulants used in agrochemicals, and evaluation of the role of these 'inerts or inactives' in pollinator decline is only in its formative stages.Effects include learning impairment for adult bees and oral toxicity for larvae and adults.Multi-billion pounds of formulation ingredients from all uses are released into US environments, making this an important component of the chemical landscape to which bees are exposed.Adjuvants and co-formulants generally greatly enhance the pesticidal efficacy and inadvertently the non-target effects of the active ingredient.Organosilicone surfactants are the most potent tank adjuvants and super-penetrants available to growers.Based on the California Dept of Pesticide Regulation data for agrochemical applications to almonds, there has been increasing use of adjuvants, particularly organosilicone surfactants, during bloom when two-thirds of USA honey bee colonies are present. Increased tank-mixing of these with fungicides and insect growth regulators may be associated with recent USA honey bee declines.Spray tank adjuvants are largely assumed to be biologically inert and are not registered by the US-EPA, leaving their regulation and monitoring to individual states.Formulation composition and not just the dose of active ingredient makes the poison.In our research, we have found adjuvants like organosiloxane, nonylphenol and octylphenol polyethoxylate surfactants and the co-solvent N-methyl-2-pyrrolidone (NMP) at ppm levels in beehive samples.We found adjuvants like organosilicone surfactants or the solvent NMP alone are orally and topically toxic to bees, but greater impacts are found on combination with other stressors including pesticides and viruses. Additionally, we found an organosilicone surfactant adjuvant frequently used during almond pollination, when combined at a field-relevant concentration with prevalent bee viruses, causes synergistic mortality in honey bee larvae.Furthermore, we demonstrated that formulations are generally more toxic than respective active ingredients, particularly fungicides, by up to 26,000-fold. Moreover, we have found 100% of co-formulants analyzed for in beehive samples, while only 70% of pesticide active ingredients searched for have been detected. We have launched a new program called Landscapes for Bees, in which we obtain data on colony health metrics and management information from beekeepers in Pa and surrounding states and determine how these correlate with generalizable indices of features in the landscape, including forage resource quality and pesticide exposure risk.Preliminary data and analyses found a strong correlation between survival and forage resource quality and Varroa management, but revealed variation in survival rates between different Pa counties that are not explained by either factor.Furthermore, our results indicate that Varroa treatments are most important in counties where survival is overall low, and do not significantly impact survival in counties where survival is overall high, suggesting interactions among these different factors.These studies are in collaboration with Eric Lonsdorf and the USDA-ERS.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 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 IPPM context, both pest management and pollinator protection may be achieved.Moreover, we are examining the factors that impact overwintering success in honey bee colonies.

Publications

  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Mullin, C. A., J. D. Fine, R. D. Reynolds and M. T. Frazier. 2016. Toxicological risks of agrochemical spray adjuvants: Organosilicone surfactants may not be safe. Frontiers in Public Health 4:1-8. Article 92.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Traynor, K. S., J. S. Pettis, D. R. Tarpy, C. A. Mullin, J. L. Frazier, M. Frazier and D. vanEngelsdorp. 2016. In-hive pesticide exposome: Assessing risks to migratory honey bees from in-hive pesticide contamination in the Eastern United States. Scientific Reports 6:33207.
  • Type: Journal Articles Status: Accepted Year Published: 2016 Citation: van Belleghem, S. M., P. Rastas, A. Papanicolaou, S.H. Martin, J.J. Hanly, J. Mallet, J.J. Lewis, H. M. Hines, M. Ruiz, G.R.P. Moreira, C.D. Jiggins, B.A. Counterman, W.O. McMillan, R. Papa. Complex modular architecture around a simple toolkit of wing pattern genes. Nature Ecology & Evolution.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Nadeau, N.J., C. Pardo-Diaz, A. Whibley, M.A. Supple, S.V. Saenko, R.W.R. Wallbank, G.C. Wu, L. Maroja, L. Ferguson, J.J. Hanly, H. Hines, C. Salazar, R.M. Merrill, A.J. Dowling, R.H. ffrench-Constant, V. Llaurens, M. Joron, W.O. McMillan, C. Jiggins. 2016. The gene cortex controls mimicry and crypsis in butterflies and moths. Nature. 543:106-110.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: L�pez-Uribe MM, Minckley RL, Cane J, Danforth BN (2016) Crop domestication facilitated rapid geographical expansion of a specialist pollinator, the squash bee Peponapis pruinosa. Proceedings of the Royal Society of London B 283:20160443. doi: 10.1098/rspb.2016.0443
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Kamvar ZN, L�pez-Uribe MM, Coughan S, Gr�nwald NJ, Lapp H, Manel S (2016) Developing educational tools for population genetics in R: a shared and interactive approach. Molecular Ecology Resources. doi: 10.1111/1755-0998.12558
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: L�pez-Uribe MM, Sconiers WB, Frank SD, Dunn RR, Tarpy DR (2016) Reduced cellular immune response in social insect lineages. Biology Letters 12:20150984. doi: 10.1098/rsbl.2015.0984
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Joshi, N. K., M. Otieno, E. G. Rajotte, S. J. Fleischer, & D. Biddinger. 2016. Proximity to woodland and landscape structure drives pollinator visitation in apple orchard ecosystem. Frontiers in Ecology and Evolution. Vol. 34(4) doi: 10.3389/fevo.2016.00038.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Joshi, N. K., B. Butler, K. Demchak, & D. Biddinger. 2016. Seasonal occurrence of spotted wing drosophila (Drosophial suzukii) in various small fruits and berries in Pennsylvania and Maryland. J. of Applied Entomol. doi: 10.1111/jen.12325
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Kammerer, M. A., D. J. Biddinger, N. K. Joshi, E. G. Rajotte, & D. Mortensen. 2016. Modeling local spatial patterns of wild bee diversity in Pennsylvania apple orchards. Landscape Ecology. Doi: 10.1007/s10980-016-0416-4.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Li, W., Evans, J.D., Huang, Q., Rodriguez-Garcia, C., Liu, J., Hamilton, M., Grozinger, C.M., Webster, T.C., Su, S., and Y-P Chen. "Silencing honey bee (Apis mellifera) naked cuticle (nkd) improves host immune function and reduces Nosema ceranae infections" Applied and Environmental Microbiology (in press), doi:10.1128/AEM.02105-16).
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Vaudo, A.D., Patch, H.M., Mortensen, D.A., Tooker, J.F., and C.M. Grozinger. "Macronutrient ratios in pollen shape bumble bee (Bombus impatiens) foraging strategies and floral preferences." Proceedings of the National Academy of Sciences 113(28):E4035E4042 (2016).
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Vaudo, A. D, Tooker, J.F., Grozinger, C.M. and H.M. Patch. "Bee nutrition and floral resource restoration." Current Opinion in Insect Science 10:133-141 (2015).
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Doke, M.A., Frazier, M. and C.M. Grozinger. "Overwintering Honey Bees: Biology and Management" Current Opinion in Insect Science 10:185-193 (2015).
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Galbraith, D.A., Kocher, S.D., Glenn, T., Albert, I., Hunt, G.J., Strassmann, J.E., Queller, D.C., and C.M. Grozinger. "Testing the kinship theory of intragenomic conflict in honey bees (Apis mellifera)." Proceedings of the National Academy of Sciences 113(4):1020-1025 (2016).
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Holt, H.L, and C.M. Grozinger. "Towards an Integrated Pest Management (IPM) approach for Nosema (Microsporidia: Nosematidae) parasites in honey bee (Hymenoptera: Apidae) colonies" Journal of Economic Entomology 109(4):1487-1503 (2016).
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Manfredini, F., Shoemaker, D., and C.M. Grozinger. "Dynamic changes in host-virus interactions associated with colony founding and social environment in fire ant queens (Solenopsis invicta)" Ecology and Evolution 6(1):233-244 (2016).
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Rittschof, C.C., Grozinger, C.M., and G.E. Robinson. "The energetic basis of behavior: bridging behavioral ecology and neuroscience" Current Opinion in Behavioral Sciences 6, 19-27 (2015).
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Amsalem, E., Grozinger, C.M., Padilla, M., and A. Hefetz. "Bumble bee sociobiology: The physiological and genomic bases of bumble bee social behavior" Advances in Insect Physiology: Genomics, Physiology and Behavior of Social Insects. Editors A. Zayed and C. Kent. Vol 48. p37-94 (2015)
  • Type: Book Chapters Status: Published Year Published: 2016 Citation: Biddinger, D., E. G. Rajotte, N. K. Joshi (2016). Integrating pollinator health into tree fruit IPM- A case study of Pennsylvania apple production (Chapter- 2). In: The pollination of cultivated plants: a compendium for practitioners (Editor- D. Roubik). FAO Book. (In Press).
  • Type: Book Chapters Status: Published Year Published: 2015 Citation: Grozinger, C.M. Honey Bee Pheromones" In: J. Graham (ed) The Hive and the Honey Bee. Indianapolis: Dadant. p311-330 (2015).
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Galbraith, G.A., Wang, Y., Page, R.E., Amdam, G. and C. M. Grozinger. "Reproductive physiology mediates honey bee (Apis mellifera) worker responses to social cues" Behavioral Ecology and Sociobiology 69 (9):1511-1518 (2015).
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Grozinger, C.M. and J.D Evans. "From the lab to the landscape: translational approaches to pollinator health". Current Opinion in Insect Science 10:vii-ix (2015).
  • Type: Journal Articles Status: Accepted Year Published: 2016 Citation: Brasero, N., B. Martinet, T. Lecocq, P. Lhomme, P. Biella, I. Valterova, K. Urbanova, M. Cornalba, H. Hines, P. Rasmont. The cephalic labial gland secretions of two socially parasitic bumble bees Bombus hyperboreus (Alpinobombus) and Bombus inexpspectatus (Thoracobombus) question their inquiline strategy. Insect Science.
  • Type: Journal Articles Status: Accepted Year Published: 2016 Citation: Miko, I, C. Trietsch, E.L. Sandall, M.J. Yoder, H.M. Hines, A. Deans. Malagasy Conostigmus (Hymenoptera: Ceraphronoidea) and the secret of the scutes. PeerJ


Progress 11/28/14 to 09/30/15

Outputs
Target Audience:Our research is targeted to multiple audiences, ranging from the general public, to bee keepers, to scientists, to government regulators at the national and international levels. In addition, we are disseminating our information to foundations, nongovernmental organizations, and to corporations who recognize an invested interest in pollinators and pollinator welfare. We have engaged in a multi-pronged effort to reach out to these groups and to disseminate our findings. All of our investigators regularly report to bee keeping clubs and organizations. We have been integrally involved in developing best management practices at the national level. Ideally and hopefully our research will lead to efforts to mitigate and improve honey bee health, along with the health of other pollinators to lead to improved environmental stability and ecosystem health. The role of these pollinators worldwide is essential for production of many different foods that provide essential nutrients and vitamins that are needed by humans and other animals. In addition, the continued stability of ecosystems depends upon flowering plant pollination that is provided via these pollinators. The impact of systemic pesticides, seed treatments, formulation additives, and other pesticides and their combinations on non-target species, and their role in honey bee andother pollinator health are of global consequence to food security and future crop protection strategies. The impacts of lack of floral resources is also of major concern for the health of honey bees and other pollinator species. Major stakeholders include the USDA, EPA, PDA, and the agrochemical industry and beekeeping organizations. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?Through this project, numerous undergraduate students, graduate students and postdocs are being trained. These includeWanyi Zhu, Michael Freiberg, Holly Holt, Jessica Richards, Gabriel Villar, Mehmet (Mali) Doke, Julia Fine, David Galbraith, Sheena Sidhu, Anthony Vaudo, SaundraWheeler, Courtnee Eddington, Briana Ezray. Current post doctoral scholars include: Jing Chen, Fabio Manfredini, David Galbraith, Claire Rittschof,and Etya Amsalem. Severalundergraduate and graduate degree courses have been created to educate students more on pollinators and issues related tothem. In addtion, we have created an annual Honey Bee Queen Rearing Workshop, which trains 14 beekeepers in honeybee queen rearing, breeding, and evaluation for productivity and disease resistance, in an effort to improve local breedingprograms. This Workshop is a cornerstone of the PA Honey Bee Stock Improvement Program, which is a partnershipbetween PA beekeepers and PSU researchers. We are currently preparing for the 3rdInternational Conference on Pollinator Biology, Health and Policy, which we anticipate will be attended by more than 250 scientists and stakeholders interested in pollinators. How have the results been disseminated to communities of interest?We have delivered numerous presentations on pollinator decline, CCD and the potential role of pesticides and co-formulants. at local, state, regional and national beekeeping conferences. In addition, we have given several presentations at scientific meetings for more than 5 different societies. What do you plan to do during the next reporting period to accomplish the goals?On each of the goals, several lines of inquiry are proceeding. These experiments not only involve honey bees, but also solitary bees and bumble bees. One of the goals is to ask if similar impacts by the various factors are seen accross the species or if some are more deeply impacted and why. It is anticipated that several major findings will be announced and published during this next reporting period.

Impacts
What was accomplished under these goals? Overall, our project as directed by 7 PI's has had significant impact on understanding some of the underlying factors impacting the health of honey bees and other pollinator species. These findings have enabled the creation of some initial best practices for those with invested interest in crop production, pollination, and apiculture. Some of these findings are highlighted below: 1)Role and causative mechanisms of parasitic mites, viruses, and microbes: Several papers were published that that immune function was being influenced by viral infections and highlighted possible pathways that may be impacted by viral infections. Studies both in Canada and Africa teased apart the interaction of mites, viruses, and nosema. It is clear that viruses can be present in honey bee colonies without having varroa mites; however, increased mite populations and parasitism are associated with higher viral prevalence and titers for several viruses. Honey bee pathogens are readily transferred both in the hive and field, and in the field these pathogens are picked up and spread by native bee communities. Native bees, however, have different life history patterns than honeybees, and the dynamics of each of these systems may influence propensity for communities to harbor pathogens. Bees with short seasonality, a harsh overwintering period, and different floral connectivity are likely to pick up and retain pathogens in different ways. It may be expected that, for example, since bumble bees must overwinter underground and this is a stressful time of their life that requires adequate food reserves, queen bees with pathogens may not successfully found colonies and thus may purge pathogens from their communities every spring. However, honeybees overwinter as colonies and may be able to retain their pathogens in the hive better than native bees. Understanding these dynamics will be important in modeling propensity for disease prevalence and transfer across communities and highlight the extent of the threat to different bee pollinators. In the last year the Hines lab has been examining the distribution of bee pathogens in bumble bees across their active season and relating this to the distribution of pathogens among honeybees in the same communities. The goal of this research is to obtain preliminary data on whether bumble bee pathogens have seasonal shifts in their abundance and distribution and to understand whether honeybees may play a role in this seasonal pattern. These bees are currently being screened for pathogens in the lab and the data will be used as preliminary data to further fund and guide the directions of this research in subsequent seasons. 2)Incorporate traits conferring resistance to parasites and pathogens: New insight has been gained into the interaction of agression with development of agression in colonies and its relationship to immune resiliency. This insight will enable future experiments to dissect out the genetic basis of these traits and their interactions. 3)Manipulation of nutrition via land management; Experiments have been performed to understand how land management practices can impact pollinator health, via nutrition alone. The Hines lab is exploring whether color intensity in bumble bees may be impacted by bee nutrition. The lab has observed marked shifts in bumble bee color during lab rearing so pursued a controlled design testing the influence of sugar source (honey/sugar), pollen quality, and environmental conditions (humity and temperature) on yellow pigment concentration in bumble bees. The goal of this research is to understand whether these bees are using evolutionary trade offs whereby they decrease pigmentation to better use these nutrients elsewhere, while also to examining whether bee color may be a bioindicator of community nutrition. 4)effects of exposure to pesticides and other xenobiotics:Honey bees are sensitive to widespread co-formulants used in agrochemicals, and evaluation of the role of these 'inerts' in pollinator decline has only begun. Effects include learning impairment for adult bees and oral toxicity for larvae and adults. Billions of pounds of formulation ingredients from all uses are released into US environments, making this an important component of the chemical landscape to which bees are exposed. Most inerts are generally considered as safe, have no mandated tolerances, and their residues are unmonitored. Lack of disclosure of co-formulants in major products, and no or inadequate methods developed for their analysis, prevents the risk evaluation of total agrochemical load for bees. Most studies to document pesticide effects on terrestrial non-targets like honey bee are performed without the formulation or other relevant spray adjuvant components used to environmentally apply the toxicant. Inerts have been found at ppm levels in hive samples. We have found that honeybees are 'poisoned' by widespread co-formulants used in agrochemicals, particularly organosilicone surfactants and the co-solvent N-methyl-2-pyrrolidone (NMP). Formulations are generally more toxic than respective active ingredients, particularly fungicides, by up to 26,000-fold based on published literature. By employing this knowledge, we can begin to optimize formulation recommendations for use in bee foraging areas. Honey bees reveal that the formulation and not just the dose makes the poison. A liquid chromatography-mass spectrometry (LC-MS) method for analysis of organosiloxane, nonylphenol and octylphenol polyethoxylate surfactants in beehive matrices was developed. A combined liquid-liquid extraction and solid phase extraction method was used. Less than 2 grams of honey, pollen or wax were extracted using the QuEChERS (Quick, Easy, Cheap, Effective, Rugged and Safe) approach. Identification and quantification were accomplished employing liquid chromatography coupled to electrospray ionization mass spectrometry. Trisiloxane surfactants were detected in every beeswax and 60% of the pollen samples. Much higher nonylphenol polyethoxylate residues levels were found in wax followed by pollen than in honey, while octylphenol polyethoxylate residues were 10 times lower in pollen and wax. A significant positive correlation was found between total concentrations of nonylphenol polyethoxylates and pesticide residues. We have also shown that chronic dietary exposure to a fungicide chlorothalonil, pesticide mixtures, and a formulation solvent have the potential to impact honey bee populations, and warrant further investigation. Most notable are the chronic larval toxicities of the fungicide chlorothalonil and its synergistic combinations with frequently used in-hive miticides, and the unexpected high toxicity of the formulation ingredient NMP. Notable findings: We have found that honeybees are 'poisoned' by widespread co-formulants used in agrochemicals, particularly organosilicone surfactants and the co-solvent N-methyl-2-pyrrolidone. We have found 100% of co-formulants analyzed for in beehive samples, while only 70% of pesticide active ingredients searched for have been detected. Formulations are generally more toxic than respective active ingredients, particularly fungicides, by up to 26,000-fold. Honey bees reveal that the formulation and not just the dose makes the poison. 5) Interaction of factors: Several experiments are underway to examine the interaction of all of the above factors. Subsets of these factors have been found to interact to negatively impact the health of colonies. These findings are being written at this time. 6) Best practices for beekeepers, growers, land managers, and homeowners: New philosophies and practices are being developed for Integrated Pest and Pollinator Management (IPPM). The goal of IPPM will be to promote the health of pollinators while controlling pests of a particular crop.

Publications

  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Chen, J. and C. A. Mullin. 2014. Determination of nonylphenol ethoxylate and octylphenol ethoxylate surfactants in beehive samples by high performance liquid chromatography coupled to mass spectrometry. Food Chem. 158:473-479.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Chen, J. and C. A. Mullin. 2015. Characterization of trisiloxane surfactants from agrochemical adjuvants and pollinator-related matrices using liquid chromatography coupled to mass spectrometry. J. Agric. Food Chem. 63:5120-5125. http://dx.doi.org/10.1021/jf505634x
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Frazier, M., C. Mullin, J. Frazier, S. Ashcraft, T. Leslie, E. Mussen and F. Drummond. 2015. Assessing honey bee (Hymenoptera: Apidae) foraging populations and the potential impact of pesticides on eight U. S. Crops. J. Econ. Entomol. 108:2141-2152. http://dx.doi.org/10.1093/jee/tov195
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Mullin, C. A. 2015. Effects of inactive ingredients on bees. Curr. Opin. Insect Sci. 10:194-200.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Mullin, C. A., J. Chen, J. D. Fine, M. T. Frazier and J. L. Frazier. 2015. The formulation makes the honey bee poison. Pestic. Biochem. Physiol. 120:27-35. http://dx.doi.org/10.1016/j.pestbp.2014.12.026
  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Zhu, W., D. R. Schmehl, C. A. Mullin and J. L. Frazier. 2014. Four common pesticides, their mixtures and a formulation solvent in the hive environment have high oral toxicity to honey bee larvae. PLoS ONE 9(1):e77547.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Fine, J. D. and C. A. Mullin. 2015. Toxicodynamics of the pesticide inert N-methyl-2-pyrrolidone and its impacts on honey bees. In: Pollinators and Agrochemical symposium, AGRO 208, 250th ACS National Meeting, Boston, MA. (Abstract)
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Mullin C., J. Chen, J. Fine, R. Reynolds and M. Frazier. 2015. Formulation composition makes the pollinator poison. In: Pollinators and Agrochemical symposium, AGRO 214, 250th ACS National Meeting, Boston, MA. (Abstract)
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Rittschof CC, Coombs CB, Frazier M, Grozinger CM, Robinson GE. Early-life experience affects honey bee aggression and resilience to immune challenge. Sci Rep. 2015 Oct 23;5:15572. doi: 10.1038/srep15572.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Amsalem E, Orlova M, Grozinger CM. A conserved class of queen pheromones? Re-evaluating the evidence in bumblebees (Bombus impatiens). Proc Biol Sci. 2015 Oct 22;282(1817). pii: 20151800. doi: 10.1098/rspb.2015.1800.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Amsalem E, Galbraith DA, Cnaani J, Teal PE, Grozinger CM. Conservation and modification of genetic and physiological toolkits underpinning diapause in bumble bee queens. Mol Ecol. 2015 Oct 10. doi:10.1111/mec.13410.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Grozinger CM, Robinson GE. The power and promise of applying genomics to honey bee health. Curr Opin Insect Sci. 2015 Aug 1;10:124-132.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Fuller ZL, Ni�o EL, Patch HM, Bedoya-Reina OC, Baumgarten T, Muli E, Mumoki F, Ratan A, McGraw J, Frazier M, Masiga D, Schuster S, Grozinger CM, Miller W. Genome-wide analysis of signatures of selection in populations of African honey bees (Apis mellifera) using new web-based tools. BMC Genomics. 2015 Jul 10;16:518. doi: 10.1186/s12864-015-1712-0.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Kocher SD, Tsuruda JM, Gibson JD, Emore CM, Arechavaleta-Velasco ME, Queller DC, Strassmann JE, Grozinger CM, Gribskov MR, San Miguel P, Westerman R, Hunt GJ. A Search for Parent-of-Origin Effects on Honey Bee Gene Expression. G3 (Bethesda). 2015 Jun 5;5(8):1657-62. doi: 10.1534/g3.115.017814.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Villar G, Baker TC, Patch HM, Grozinger CM. Neurophysiological mechanisms underlying sex- and maturation-related variation in pheromone responses in honey bees (Apis mellifera). J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2015 Jul;201(7):731-9. doi: 10.1007/s00359-015-1006-7.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Galbraith DA, Yang X, Ni�o EL, Yi S, Grozinger C. Parallel epigenomic and transcriptomic responses to viral infection in honey bees (Apis mellifera). PLoS Pathog. 2015 Mar 26;11(3):e1004713. doi: 10.1371/journal.ppat.1004713. eCollection 2015 Mar.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Condamine FL, Hines HM. Historical species losses in bumblebee evolution. Biol Lett. 2015 Mar;11(3). pii: 20141049. doi: 10.1098/rsbl.2014.1049.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Deans AR, Lewis SE, Huala E, Anzaldo SS, Ashburner M, Balhoff JP, Blackburn DC, Blake JA, Burleigh JG, Chanet B, Cooper LD, Courtot M, Cs�sz S, Cui H, Dahdul W, Das S, Dececchi TA, Dettai A, Diogo R, Druzinsky RE, Dumontier M, Franz NM, Friedrich F, Gkoutos GV, Haendel M, Harmon LJ, Hayamizu TF, He Y, Hines HM, Ibrahim N, Jackson LM, Jaiswal P, James-Zorn C, K�hler S, Lecointre G, Lapp H, Lawrence CJ, Le Nov�re N, Lundberg JG, Macklin J, Mast AR, Midford PE, Mik� I, Mungall CJ, Oellrich A, Osumi-Sutherland D, Parkinson H, Ram�rez MJ, Richter S, Robinson PN, Ruttenberg A, Schulz KS, Segerdell E, Seltmann KC, Sharkey MJ, Smith AD, Smith B, Specht CD, Squires RB, Thacker RW, Thessen A, Fernandez-Triana J, Vihinen M, Vize PD, Vogt L, Wall CE, Walls RL, Westerfeld M, Wharton RA, Wirkner CS, Woolley JB, Yoder MJ, Zorn AM, Mabee P. Finding our way through phenotypes. PLoS Biol. 2015 Jan 6;13(1):e1002033. doi: 10.1371/journal.pbio.1002033.
  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Keith DA, Mahony M, Hines H, Elith J, Regan TJ, Baumgartner JB, Hunter D, Heard GW, Mitchell NJ, Parris KM, Penman T, Scheele B, Simpson CC, Tingley R, Tracy CR, West M, Ak�akaya HR. Detecting extinction risk from climate change by IUCN Red List criteria. Conserv Biol. 2014 Jun;28(3):810-9. doi:10.1111/cobi.12234.
  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Muli E, Patch H, Frazier M, Frazier J, Torto B, Baumgarten T, Kilonzo J, Kimani JN, Mumoki F, Masiga D, Tumlinson J, Grozinger C. Evaluation of the distribution and impacts of parasites, pathogens, and pesticides on honey bee (Apis mellifera) populations in East Africa. PLoS One. 2014 Apr 16;9(4):e94459. doi: 10.1371/journal.pone.0094459.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Melanie A Kammerer, David J Biddinger, Edwin G Rajotte, David A Mortensen: Local Plant Diversity Across Multiple Habitats Supports a Diverse Wild Bee Community in Pennsylvania Apple Orchards. Environmental Entomology 09/2015; DOI:10.1093/ee/nvv147
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: David J. Biddinger, Edwin G. Rajotte 2015. Integrated Pest and Pollinator Management  Adding a New Dimension To An Accepted Paradigm. Current Opinion in Insect Science. 06/2015; 10. DOI:10.1016/j.cois.2015.05.012
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Joshi, Neelendra K. , Timothy Leslie, Edwin George Rajotte, Melanie Kammerer, Mark Otieno and David Biddinger 2015. Comparative Trapping Efficiency to Characterize Bee Abundance, Diversity and Community Composition in Apple Orchards. ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA � MAY 2015. DOI: 10.1093/aesa/sav057.
  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Shutler D, Head K, Burgher-MacLellan KL, Colwell MJ, Levitt AL, Ostiguy N, Williams GR. Honey bee Apis mellifera parasites in the absence of Nosema ceranae fungi and Varroa destructor mites. PLoS One. 2014 Jun 23;9(6):e98599. doi:10.1371/journal.pone.0098599.
  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Chejanovsky N, Ophir R, Schwager MS, Slabezki Y, Grossman S, Cox-Foster D. Characterization of viral siRNA populations in honey bee colony collapse disorder. Virology. 2014 Apr;454-455:176-83. doi: 10.1016/j.virol.2014.02.012.