Source: UNIV OF MINNESOTA submitted to NRP
IMPROVING THE HEALTH AND MANAGEMENT PRACTICES OF HONEY BEES
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
COMPLETE
Funding Source
Reporting Frequency
Annual
Accession No.
1010304
Grant No.
(N/A)
Cumulative Award Amt.
(N/A)
Proposal No.
(N/A)
Multistate No.
(N/A)
Project Start Date
Oct 1, 2016
Project End Date
Sep 30, 2021
Grant Year
(N/A)
Program Code
[(N/A)]- (N/A)
Recipient Organization
UNIV OF MINNESOTA
(N/A)
ST PAUL,MN 55108
Performing Department
Entomology
Non Technical Summary
The main goal of this project is to improve the health and management practices of honey bee colonies, and to ensure the research results are effectively translated to beekeepers, growers of bee-pollinated crops, and the public. Since 2006, an average of 35% of all honey bee colonies die across the nation from multiple and interacting causes, including pathogens, parasites, pesticides and poor nutrition due to lack of floral resources. In Minnesota, the average mortality of colonies from in 2014-2015 reached a record high of 51%. It is critical to restore honey bee health and economic vitality to the beekeeping industry. Using novel approaches, we will explore honey bees' natural defenses against parasites and diseases, breed bees to enhance these traits, and develop ways to improve the overall management practices of honey bee colonies. The three objectives of this research are to: 1) Explore how honey bees select and exploit the pharmacological properties of plant resins (propolis) to benefit the health of the colony; 2) Select honey bee colonies for high hygienic behavior and resin (propolis) collection and breed a line of bees that expresses both traits; and 3) Continue extension and outreach programming for commercial and backyard beekeepers.
Animal Health Component
50%
Research Effort Categories
Basic
50%
Applied
50%
Developmental
(N/A)
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
31530101060100%
Goals / Objectives
The main goal of this project is to improve the health and management practices of honey bee colonies, and to ensure our research results are effectively translated to beekeepers, growers of bee-pollinated crops, and the public. The basic and applied experimental approaches for the next five years are as follows:Objective 1. Explore how honey bees select and exploit the pharmacological properties of plant resins (propolis) to benefit the health of the colony.Objective 2. Select honey bee colonies for high hygienic behavior and resin (propolis) collection and breed a line of bees that expresses both traits.Objective 3. Continue extension and outreach programming for commercial and backyard beekeepers
Project Methods
Objective 1. The first set of experiments will test if resin-foraging bees have greater olfactory sensitivity and responsiveness to volatiles associated with fungal microorganisms compared to volatiles associated with bacterial microorganisms. For these tests we will use proboscis-extension response (PER) conditioning, a technique previously used in the Spivak lab to reveal olfactory and tactile responsiveness of hygienic and resin collecting honey bees. We will present dilutions of these three compounds, phenethyl acetate, 2-phenylethanol, and benzyl alcohol (associated with diseased brood caused by fungal pathogen Ascosphaera apis) individually to resin and pollen foragers to determine if resin foragers learn to associate the disease odors with a sucrose reward (CS+ conditioned stimulus) better than pollen foragers. We also will test if resin foragers can discriminate between the odors of live 5th instar larvae infected with A. apis as the CS+ and same-age larvae infected with P. larvae as the CS- (unconditioned stimulus), and vice versa. Learning curves to the CS+ will be analyzed using logistic growth curve analysis, and discrimination scores (subtracting total number of responses to CS- from responses to CS+) will be compared using a Wilcoxon rank sum test to analyze results from discrimination conditioning. Finally, we will present 1) live spores of A. apis, 2) heat-killed spores of A. apis, 3) spores of the non-honey bee pathogen Metarhizium anopsilae, and 4) the most relevant volatiles to live colonies. We will compare the number of resin foragers returning to the colony before and after presentation to quantify if they increase resin collection due to handling of spores or simply due to exposure to its volatiles.The second set of experiments for Objective 1 will test the role of volatile olfactory cues in the ability of honey bees to locate sources of plant resins in the environment. We will present choice tests to small colonies of bees individually (5 combs per colony) derived from A. m. caucasica and A. m. ligustica (headed by sister queens to reduce genetic variability within types) in outdoor, contained flight tunnels. First, known quantities of resins collected from different trees will be placed in separate petri dishes at least 1m apart. The number of foragers from one colony at a time that land on and/or collect resin from each dish will be recorded. Handling time will be recorded for bees that load resin onto their corbiculae to test for ease of collection of different resin types. Resin pairs will include Populus deltoides and Picea glauca, and other resins of known antimicrobial activity. We will also present volatile fractions to foraging honey bees, and the antimicrobial activity of the most attractive volatile components will be determined using a variation on our well established high-throughput assay. Objective 2. Selection for hygienic behavior involves freeze-killing (with liquid nitrogen) a known number of pupae within a comb, and quantifying the time it takes the colony to remove the dead pupae from the cells (reviewed in Wilson-Rich et al., 2009). Colonies that remove over 95% of the freeze-killed brood within 24 hours are considered hygienic. Rapid removal of freeze-killed is correlated with removal of diseased and parasitized brood. Beginning with colonies already bred for high hygienic behavior (obtained from commercial beekeepers), we will house them in bee boxes fitted with propolis traps (commercially available plastic sheets with 7mm slits) stapled to the four inner walls of each box. The gaps in the traps induce bees to fill them with propolis (Borba et al., 2015). Colonies that fill the trap within a certain time frame (e.g., 2-3 weeks) will be selected.Queen bees will be reared from colonies that display rapid hygienic behavior and high propolis collection. Queens will be artificially inseminated with 8 μl semen collected from drones from other colonies that display both traits. A minimum of 10 sublines (queen lines) with at least 10 colonies per subline, will be maintained in a semi-closed population breeding program, as was done to breed the MN Hygienic line. Each year the highest performing colonies from each subline will be selected for propogation, and results of assays for hygienic behavior and propolis collection of daughter colonies will be compared to colonies selected only for hygienic behavior, and to unselected colonies. After three years of selection, daughter queens from the line will be given to commercial beekeepers to test in their operations to ensure the colonies have high honey production, winter successfully, and significantly reduced levels of Varroa destructor parasitic mites and clinical signs of American foulbrood and chalkbrood, compared to control (unselected) colonies, using methods described in Spivak and Reuter (2001a, b).Objective 3. Given the serious and chronic health problems facing bees and the increasing demand for pollination services, we have developed a way to provide commercial beekeepers with assistance to help them maintain healthy colonies. In collaboration with the Bee Informed Partnership (a 5 year Extension grant from USDA-NIFA to Dr. D. vanEngelsdorp, UMD; www.beeinformed.org) we formed "Tech-Transfer Teams," composed of independent and experienced professional consultants, to provide on-the-ground assistance to migratory beekeepers and bee breeders. The Tech Team services include 1) testing for Nosema, Varroa, and viruses to reduce treatments for these problems when feasible; 2) providing assistance with selective breeding for colonies that display disease and mite resistance; 3) surveying beekeepers about management; and 4) providing emergency response to beekeepers in need. Working with large-scale bee breeders to help them select for both hygienic behavior and propolis collection will impact all US beekeepers that purchase genetic stock (queen bees) from these producers. In turn, this work will benefit the nation through increasing the number of colonies available for pollination and queen production, and reducing the spread of diseases and parasites.To assist backyard beekeepers, we initiated a very successful fee-based extension program within M. Spivak's bee lab called the Bee Squad. (www.beelab.umn.edu). The Bee Squad, coordinated by Dr. Becky Masterman, provides personalized, hands-on training for new and experienced urban beekeepers to ensure sound beekeeping practices. They also provide full beekeeping service for homeowners and commercial businesses that want bee hives on their property but do not want the responsibility of managing the bees. Information on bee health in the Twin Cities will be fed into national bee health database (www.beeinformed.org). Another goal of the Bee Squad is to increase the availability of habitat for bees by promoting nesting sites for wild bees, and encouraging homeowners and businesses to plant bee-friendly gardens, bee lawns, and roadsides. The fees for service and other generous donations support the salaries and expenses of Bee Squad employees. The Bee Squad model is being considered for adoption at other Universities across the nation with active bee extension programs.

Progress 10/01/16 to 09/30/21

Outputs
Target Audience:Target audience are beekeepers (backyard, small scale and large scale commercial), bee breeders, the public interested in improving flowering landscapes to provide nutritional resources for bee health, and pesticide applicators (commercial and homeowners) to help mitigate effects of toxic pesticides on bee health and survival. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?Currently, this research is providing trainingcurrent graduate student(M. Shanahan) and a post-doctoral researcher, Sofia Levin, who arestudying the benefits of propolis to honey bee health. Two technicians provide honey bee management and data collection support for research colonies. One technician assists with molecular studies in the lab. One Tech Transfer Team member is currently employed to survey honey bee colonies in commercial apiaries in Upper Midwest. Five full or part time people are employed through the Bee Squad program to assist backyard beekeepers in the Twin Cities area How have the results been disseminated to communities of interest?Peer reviewed research publications, extension publications, web-based materials, videos, books, talks at local, regional, national and international conferences and seminars, and one-on-one training to beekeepers in the field. What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? Objective 1.We are making good progress in selecting colonies for resistance to Varroa mites, by evaluating colonies from honey bee stocks derived from A. mellifera ligustica and carnica. We are evaluating colonies for wintering survivorship (frames of bees and brood in early spring) and for three behavioral traits that help bees defend against pathogens and parasites: high propolis collection (quantified using propolis traps), rapid hygienic behavior (quantified using the freeze-killed brood assay), and low Varroa mite population growth over the season (comparing the proportion of mites in worker brood over time). We have identified over 50 colonies that score in our top tier that comprise the breeding stock for future generations. Results: Spivak co-authored a paper (K. Wagoner was first author) on the results from a chemical assay to test colonies for their hygienic response to Varroa infested brood, Key outcomes: Selecting new lines of bees for propolis collection, hygienic behavior, and reduced mite population growth should, in the long-term, result in colonies more able to defend themselves against various parasites and pathogens, and should result in beekeepers having to use fewer chemical treatments to keep colonies alive. Objective 2. Major activities completed: We have submitted for publication our findings on how "Bee Lawns" (the introduction of low-growing flowers within turfgrass lawn), can support pollinator diversity and reduce inputs, while maintaining the traditional aesthetics and recreational uses associated with lawns. Results: In the bee lawns established in Minneapolis parks, we found 56 species of bees on Trifolium repens, with A. mellifera as the most common species observed. The addition of native Prunella vulgaris increased bee diversity significantly compared to lawns seeded with just T. repens. Key Outcomes: This study has generated a huge interest across the state of Minnesota, even leading to a legislative initiative called "Lawns to Legumes" program that offers a combination of workshops, coaching, planting guides and cost-share funding for installing pollinator-friendly native plantings in residential lawns in Minnesota. Objective 3. Major activities completed and reported in previous reports. Objective 4.Tech Transfer Team member, Nelson Williams, sampled over 600 commercial honey bee colonies from over 30 operations in MN, WI and ND, using standard metrics to assess bee health, to contribute to the national database on honey bee health. The Bee Squad, the outreach arm of the Bee Lab, taught over 50 hands-on classes to local Twin Cities beekeepers between April and October, and monitored the health of eight apiaries, using the same metrics as used in commercial colonies. The Bee Squad also continued to teach hands-on beekeeping classes to war veterans, and to offenders in minimum-security prisons. Results: The results of Tech Team sampling were first submitted to the individual beekeepers to help inform management and treatment decisions in their operations. The health metrics collected by the Tech Team and the Bee Squad were also submitted to the Bee Informed Partnership national database, where they are summarized and used in meta-analysis to summarize regional trends in honey bee health, and management suggestions to improve colony health. Key outcomes: Simple metrics can be used by beekeepers to inform management and treatment decisions with the goal of increasing the health and survivorship of honey bee colonies locally and in the Upper Midwest. Training new beekeepers ensures they promote honey bee health; training veterans and offenders in beekeeping provides trade and income opportunities through honey production.

Publications

  • Type: Journal Articles Status: Published Year Published: 2021 Citation: Wagoner K, Miller JG, Keller J, Bello J, Waiker P, Schal, Spivak M. Rueppell O. 2021. Hygiene-eliciting brood semiochemicals as a tool for assaying honey bee (Hymenoptera: Apidae) colony resistance to Varroa (Mesostigmata: Varroidae). J. Insect Sci. 21( 6) 4, doi.org/10.1093/jisesa/ieab064
  • Type: Journal Articles Status: Published Year Published: 2021 Citation: Shanahan M, Spivak M. 2021. Resin use by stingless bees: A review. Insects. 12, 719. https://doi.org/10.3390/insects12080719
  • Type: Journal Articles Status: Published Year Published: 2021 Citation: Kulhanek K, Steinhauer N, Wilkes J, Wilson M, Spivak M, Sagili RR, et al. 2021. Survey-derived best management practices for backyard beekeepers improve colony health and reduce mortality. PLoS ONE 16(1): e0245490. https://doi.org/10.1371/journal.pone.0245490
  • Type: Other Status: Published Year Published: 2021 Citation: Spivak, M. 2021. Double-Edged Swords. American Bee Journal 161(10):1135-1136.


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

Outputs
Target Audience:Target audiences arebeekeepers (backyard, small scale and large scale commercial), and bee breeders to help improve bee health. Other audiences include researchers and other academics, the public, and policy makersinterested in improving flowering landscapes to provide nutritional resources for bee health. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?This research is providing training for two current graduate students (M. Shanahan, H. Dalenberg), one undergraduate, and one post-doctoral researcher (M. Goblirsch). Three technicians provide honey bee management and data collection support for research colonies. One technician assists with molecular studies in the lab. One Tech Transfer Team member is currently employed to survey honey bee colonies in commercial apiaries in Upper Midwest. Five full or part time people are employed through the Bee Squad program to assist backyard beekeepers in the Twin Cities area. How have the results been disseminated to communities of interest?M. Spivak presented these findings at over 24 scientific and beekeeping conferences locally, regionally, nationally and internationally, including presentations in the UK, Australia, Brazil, as well as the American Bee Research Conference and other beekeeping groups in the U.S. Research findings have been published in peer-reviewed journal, and announced through social media (www.facebook.com/umnBeeLab/ and www.facebook.com/umnBeeSquad) What do you plan to do during the next reporting period to accomplish the goals?We will continue proposed research and extension efforts as proposed, with no changes.

Impacts
What was accomplished under these goals? Impact. The main goals of this project are to improve the health and management practices of honey bee colonies, and to ensure the research results are effectively translated to beekeepers, growers of bee-pollinated crops, and the public. It is critical to restore honey bee health and economic vitality to the beekeeping industry. Using novel approaches, we are exploring honey bees' natural defenses against parasites and diseases, breed bees to enhance these traits, and develop ways to improve the overall management practices of honey bee colonies. Objective 1. Major activities completed, Data collected: Graduate student Maggie Shanahan, in collaboration with Dr. Mike Simone-Finstrom conducted a second year of study to determine 1) what surface textures inside standard beekeeping boxes promote propolis collection by bees, and 2) how much propolis is needed to provide immune support to individual bees in a colony. Standard indicators of colony health were measured, and bee samples are currently being analyzed to test immune gene expression using quantitative PCR techniques. M. Shanahan also collected data on the effects of propolis on the melanization response of honey bees, another immune response. Preliminary findings indicate propolis may inhibit the melanization response, but experiments need to be replicated. Dr. Mike Goblirsch, former post-doc in Spivak's lab and now Researcher at USDA-ARS in Missisippi, continued testing if propolis inhibits viral replication in honey bee cells in vitro; preliminary data suggest propolis may affect Acute Bee Paralysis virus, but this finding will be repeated to verify. Results. Graduate student Hollie Wall-Dalenberg, in collaboration with Dr. Kirk Anderson of USDA-ARS Tucson, AZ, published a study in the journalInsects on the effects of propolis on the microbiome of honey bee mouthparts. Bee mouthparts are important because they are the interface between the external hive environment and internal bee environment. Exposure to propolis changed the microbe community composition on the mouthparts: Bees exposed to propolis had a significantly higher abundance of the core bacterial species typically associated with the bee microbiome, and lower diversity of bacteria because there were fewer opportunistic and pathogenic bacteria. The results from this microbiome experiment help explain the mode of action of propolis on honey bee immune function; that is, the antimicrobial effects of propolis reduce the opportunistic and pathogenic microbe load in the nest which subsequently reduces the need for honey bees to activate their immune responses. The same results were found in a separate study by Saelao et al. in thejournalBiology Letters on the effects of propolis on the gut microbiome. Key outcomes: Researchers and beekeepers are starting to understand how propolis improves immune function and disease resistance in honey bee colonies and are beginning to explore ways to encourage colonies to construct a propolis envelope within beekeeping equipment. This is a major change in perception and behavior because beekeepers have long considered propolis a sticky nuisance within bee colonies, and researchers had not understood the importance of the antimicrobial properties to bee health. The findings will reveal novel approaches to promote honey bee health, define at a fundamental level the use of naturally collected compounds in mitigating disease, and potentially reduce unsustainable colony losses nationwide. Objective 2. Major activities; Data collected: We continue evaluating colonies from honey bee stocks derived from A. mellifera ligustica and carnica by scoring them for wintering survivorship (frames of bees and brood in early spring) and for three behavioral traits that help bees defend against pathogens and parasites: high propolis collection (quantified using propolis traps), rapid hygienic behavior (quantified using the freeze-killed brood assay), and low Varroa mite population growth over the season (comparing the proportion of mites in worker brood over time). We have identified over 35 colonies that score in our top tier and if they survive winter 2020-21, we will breed another generation from them next summer.Results: Spivak published an invited review article on hygienic behavior for Apidologie.Key outcomes: Selecting new lines of bees for propolis collection, hygienic behavior, and reduced mite population growth should, in the long-term, result in colonies more able to defend themselves against various parasites and pathogens, and should result in beekeepers having to use fewer chemical treatments to keep colonies alive. Objective 3: Major activities completed, Data collected: We continue our extension and outreach programming for commercial and backyard beekeepers. Tech Transfer Team member, Nelson Williams, sampled over 500 commercial honey bee colonies from over 30 operations in MN, WI and ND, using standard metrics to assess bee health, to contribute to the national database on honey bee health. The Bee Squad, the outreach arm of the Bee Lab, taught over 50 hands-on classes to local Twin Cities beekeepers between April and October, and monitored the health of over 50 colonies, using the same metrics as used in commercial colonies. The Bee Squad also continued to teach hands-on beekeeping classes to war veterans, and to offenders in minimum-security prisons.Results: The results of Tech Team sampling were first submitted to the individual beekeepers to help inform management and treatment decisions in their operations. The health metrics collected by the Tech Team and the Bee Squad were also submitted to the Bee Informed Partnership national database, where they are summarized and used in meta-analysis to summarize regional trends in honey bee health, and management suggestions to improve colony health.Key outcomes: Simple metrics can be used by beekeepers to inform management and treatment decisions with the goal of increasing the health and survivorship of honey bee colonies locally and in the Upper Midwest. Training new beekeepers ensures they promote honey bee health; training veterans and offenders in beekeeping provides trade and income opportunities through honey production. Key outcomes: Simple metrics can be used by beekeepers to inform management and treatment decisions with the goal of increasing the health and survivorship of honey bee colonies locally and in the Upper Midwest. Training new beekeepers ensures they promote honey bee health; training veterans and offenders in beekeeping provides trade and income opportunities through honey production.

Publications

  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Spivak M, Danka RG. 2020. Perspectives on hygienic behavior in Apis mellifera and other social insects. Apidologie DOI: 10.1007/s13592-020-00784-z
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Goblirsch M, Warner JF, Sommerfeldt BA, Spivak M. 2020. Social fever or general immune response? Revisiting an example of social immunity in honey bees. Insects 11: 528 doi:10.3390/insects11080528
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Dalenberg H, Maes P, Mott B, Anderson KE, Spivak M. 2020. Propolis envelope promotes beneficial bacteria in the honey bee (Apis mellifera) mouthpart microbiome. Insects 11, 453. doi:10.3390/insects1107/0453
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Saelao P, Borba RS, Ricigliano V, Spivak M, Simone-Finstrom M. 2020. Honeybee microbiome is stabilized in the presence of propolis. Biology Letters 16: 202003. doi.org/10.1098/rsbl.2020.0003
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Carr-Markell MK, Demler CM, Cuvillon MJ, Schurch R, Spivak, M. 2020. Do honey bee (Apis mellifera) foragers recruit their nestmates to native forbs in reconstructed prairie habitats? PlosOne. 15(2): e0228169. https://doi.org/10.1371/ journal.pone.0228169
  • Type: Book Chapters Status: Published Year Published: 2020 Citation: Spivak M, Simone-Finstrom M. 2019. Propolis. In: Starr C. (eds) Encyclopedia of Social Insects. Springer, Cham. https://doi.org/10.1007/978-3-319-90306-4_134-1


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

Outputs
Target Audience:Target audiences arebeekeepers (backyard, small scale and large scale commercial), and bee breeders to help improve bee health. Other audiences include researchers and other academics, the public, and policy makersinterested in improving flowering landscapes to provide nutritional resources for Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?This research is providing training for two current graduate students (M. Shanahan, H. Dalenberg), one undergraduate, and one post-doctoral researcher (M. Goblirsch). Three technicians provide honey bee management and data collection support for research colonies. One Tech Transfer Team member is currently employed to survey honey bee colonies in commercial apiaries in Upper Midwest. Five full or part time people are employed through the Bee Squad program to assist backyard beekeepers in the Twin Cities area. How have the results been disseminated to communities of interest?M. Spivak presented these findings at over 10 scientific and beekeeping conferences locally, regionally, nationally and internationally, including keynote presentations to Apimondia (International Bee Conference) in Montreal, Canada; the University of Missouri, Department of Biology CV Riley Lecture Series, and the International Union for the Study of Social Insects, European Section. Post-doctoral researchers and graduate students presented findings at an additional 10 scientific and beekeeping conferences, including talks at the Entomological Society of America and the American Bee Research Conferences. A field day was hosted to demonstrate to public land managers of parks and public places in Twin Cities areas how to install and maintain "bee lawns" or flowering lawns to provide floral resources for pollinators. We published 3 articles related to the bee lawn research. What do you plan to do during the next reporting period to accomplish the goals?We will continue proposed research and extension efforts as proposed, with no changes.

Impacts
What was accomplished under these goals? Impact.The main goals of this project are to improve the health and management practices of honey bee colonies, and to ensure the research results are effectively translated to beekeepers, growers of bee-pollinated crops, and the public. It is critical to restore honey bee health and economic vitality to the beekeeping industry. Using novel approaches, we are exploring honey bees' natural defenses against parasites and diseases, breed bees to enhance these traits, and develop ways to improve the overall management practices of honey bee colonies. Objective 1.Major activities completed, Data collected: Graduate student Maggie Shanahan, in collaboration with Dr. Mike Simone-Finstrom conducted a second year of study to determine 1) what surface textures inside standard beekeeping boxes promote propolis collection by bees, and 2) how much propolis is needed to provide immune support to individual bees in a colony. Standard indicators of colony health were measured, and bee samples are currently being analyzed to test immune gene expression using quantitative PCR techniques. Graduate student Hollie Wall-Dalenberg, in collaboration with Dr. Kirk Anderson of USDA-ARS Tucson, AZ, conducted studies on the effects of propolis on the microbiome of honey bee mouthparts by exposing bees in cages to propolis and extracting DNA from their mouthparts. Bee mouthparts are important because they are the interface between the external hive environment and internal bee environment. The DNA was sequenced by Dr. Anderson and was compared to DNA from bees not exposed to propolis. The results indicated that exposure to propolis changed the microbe community composition on the mouthparts: Bees exposed to propolis had a significantly higher abundance of the core bacterial species typically associated with the bee microbiome. The diversity of bacteria on the mouthparts of bees exposed to propolis was significantly lower because there were fewer opportunistic and pathogenic bacteria, which allowed the core species to grow. The findings are being written up for publication. The results from this microbiome experiment help explain the mode of action of propolis on honey bee immune function; that is, the antimicrobial effects of propolis reduce the opportunistic and pathogenic microbe load in the nest which subsequently reduces the need for honey bees to activate their immune responses. Post-doctoral researcher Mike Goblirsch continuedtesting if propolis can inhibit viral replication in honey bee cellsin vitro; studies are ongoing, however preliminary results indicate propolis does not inhibit Deformed Wing Virus in cell culture.Key outcomes:Researchers and beekeepers are starting to understand how propolis improves immune function and disease resistance in honey bee colonies and are beginning to explore ways to encourage colonies to construct a propolis envelope within beekeeping equipment. This is a major change in perception and behavior because beekeepers have long considered propolis a sticky nuisance within bee colonies, and researchers had not understood the importance of the antimicrobial properties to bee health. The findings will reveal novel approaches to promote honey bee health, define at a fundamental level the use of naturally collected compounds in mitigating disease, and potentially reduce unsustainable colony losses nationwide. We published a review article on Social Medication by Bees, which includes our findings on the benefits of propolis to honey bee health. Objective 2.Major activities; Data collected: We began evaluating colonies from honey bee stocks derived fromA. mellifera ligustica and carnicaby scoring them for honey production (kg produced), and wintering survivorship (frames of bees and brood in early spring). From the top scoring colonies, we conducted additional assays for three behavioral traits that help bees defend against pathogens and parasites: high propolis collection (quantified using propolis traps), rapid hygienic behavior (quantified using the freeze-killed brood assay), and lowVarroamite population growth over the season (comparing the proportion of mites in worker brood over time). M. Spivak instrumentally inseminated over 50 queen bees raised from the top performing colonies, and we will continue to evaluate and select the top performing colonies in 2020.Results: We published one peer-review article on new chemical assays for hygienic behavior, and another on indicators of queen bee quality.Key outcomes: Selecting new lines of bees for propolis collection, hygienic behavior, and reduced mite population growth should, in the long-term, result in colonies more able to defend themselves against various parasites and pathogens, and should result in beekeepers having to use fewer chemical treatments to keep colonies alive. Objective 3:Major activities completed, Data collected: Continue extension and outreach programming for commercial and backyard beekeepers Tech Transfer Team member, Nelson Williams, sampled over 500 commercial honey bee colonies from over 30 operations in MN, WI and ND, using standard metrics to assess bee health, to contribute to the national database on honey bee health. The Bee Squad, the outreach arm of the Bee Lab, taught over 50 hands-on classes to local Twin Cities beekeepers between April and October, and monitored the health of eight apiaries, using the same metrics as used in commercial colonies. The Bee Squad also continued to teach hands-on beekeeping classes to war veterans, and to offenders in minimum-security prisons.Results: The results of Tech Team sampling were first submitted to the individual beekeepers to help inform management and treatment decisions in their operations. The health metrics collected by the Tech Team and the Bee Squad were also submitted to the Bee Informed Partnership national database, where they are summarized and used in meta-analysis to summarize regional trends in honey bee health, and management suggestions to improve colony health. Key outcomes: Simple metrics can be used by beekeepers to inform management and treatment decisions with the goal of increasing the health and survivorship of honey bee colonies locally and in the Upper Midwest. Training new beekeepers ensures they promote honey bee health; training veterans and offenders in beekeeping provides trade and income opportunities through honey production.

Publications

  • Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Wagoner K, Spivak M, Hefetz A, Reams R, Rueppell O. 2019. Stock-specific chemical brood signals are induced by Varroa and Deformed Wing Virus, and elicit hygienic respons in the honey bee. Sci Reports. 9:8753. doi.org/10.1038/s41598-019-45008-2
  • Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Spivak M, Goblirsch, M, Simone-Finstrom M. 2019. Social-medication in bees: The line between individual and social regulation. Curr. Opinion Insect Science 33:49-55. https://doi.org/10.1016/j.cois.2019.02.009
  • Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Ostiguy N, Drummond FA, Aronstein K, Eitzer B, Ellis JD, Spivak M, Sheppard WS. 2019. Pesticide exposure to honey bees in a four-year nationwide study. Insects, 10, 13, doi:10.3390/insects10010013
  • Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Lane IG, Wolfin J, Watkins E, Spivak M. 2019. Testing the establishment of eight forbs in mowed lawns of hard fescue (Festuca brevipila) for use in pollinator conservation. Hort Sci. 54(12): 21-50-2155. doi.org/10.21273/HORTSCI14336-19
  • Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Lane I, Watkins E, Spivak M. 2019. Flowering Lawns: How turfgrass species and seeding rate affect establishment and bloom of a model forb, Trifolium ambiguum. Hort Science 54(5): 824-828. https://doi.org/10.21273/HORTSCI13779-18
  • Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Ramer H, Nelson K, Spivak M, Watkins E, Wolfin J, Pulscher M. 2019. Exploring park visitor perceptions of 'flowering bee lawns' in neighborhood parks in Minneapolis, MN, US. Landscape and Urban Planning.189: 117-128. https://doi.org/10.1016/j.landurbplan.2019.04.015
  • Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Lee, KV, Goblirsch M, McDermott E, Tarpy DR, Spivak M. 2019. Is the brood patterns within a honey bee colony a reliable indicator of queen quality? Insects 10, 12; doi:10.3390/insects10010012


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

Outputs
Target Audience:Target audiences arebeekeepers (backyard, small scale and large scale commercial), and bee breeders to help improve bee health. Other audiences include researchers and other academics, the public, and policy makersinterested in improving flowering landscapes to provide nutritional resources for bee health. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?This research is providing training for three graduate students (K. Lee, M. Shanahan, H. Dalenberg), three undergraduates, and two post-doctoral researchers (M. Goblirsch, and M. Wilson). In addition, two Tech Transfer Team members are employed to survey honey bee colonies in commercial apiaries. Five full or part time people are employed through the Bee Squad program to assist backyard beekeepers in the Twin Cities area. How have the results been disseminated to communities of interest?M. Spivak presented these findings at over 10 scientific and beekeeping conferences locally, regionally, nationally and internationally, including keynote presentations to the Italian National Beekeeping Conference in Paestum, Italy in March, and the 2ndInternational Congress on Propolis for Bee and Human Health in Sofia, Bulgaria in September 2018. Post-doctoral researchers and graduate students presented findings at an additional 20 scientific and beekeeping conferences, including talks at the Entomological Society of America and the American Bee Research Conferences. A field day was hosted by the Bee Squad - the extension arm of the Bee Lab in the Department of Entomology, UMN - to foster communication between beekeepers and growers on how to protect pollinators while ensuring crop production. Two extension publications were disseminated on the Bee Lab website:www.beelab.umn.edu, where all other peer-reviewed publications are posted. What do you plan to do during the next reporting period to accomplish the goals?We will continue proposed research and extension efforts as proposed, with no changes.

Impacts
What was accomplished under these goals? Impact. The main goals of this project are to improve the health and management practices of honey bee colonies, and to ensure the research results are effectively translated to beekeepers, growers of bee-pollinated crops, and the public. It is critical to restore honey bee health and economic vitality to the beekeeping industry. Using novel approaches, we are exploring honey bees' natural defenses against parasites and diseases, breed bees to enhance these traits, and develop ways to improve the overall management practices of honey bee colonies. Objective 1. Major activities completed, Data collected: Graduate student Maggie Shanahan, in collaboration with Dr. Mike Simone-Finstrom initiated a study to determine 1) what surface textures inside standard beekeeping boxes promote propolis collection by bees, and 2) how much propolis is needed to provide immune support to individual bees in a colony. Standard indicators of colony health were measured, and bee samples are currently being analyzed to test immune gene expression using quantitative PCR techniques. Graduate student Hollie Wall-Dalenberg, in collaboration with Dr. Kirk Anderson of USDA-ARS Tucson, AZ, initiated studies on the effects of propolis on the microbiome of honey bees by exposing bees in cages to propolis and extracting DNA from their mouthparts. The DNA is being sequenced by Dr. Anderson, and compared to DNA from bees not exposed to propolis. It is expected that exposure to propolis may change microbe community composition on the mouthparts that come into contact with the external hive environment and internal bee environment. Post-doctoral researcher Mike Wilson explored the mode of action of propolis on honey bee immune function to understand whether the antimicrobial effects of propolis acts directly to lower immune activation of bees, or indirectly by reducing microbe load in the nest which subsequently reduces immune activation. He exposed bees in cages to propolis or without propolis, and is measuring immune gene transcript abundance using real-time qPCR. Post-doctoral researcher Mike Goblirsch began testing if propolis can inhibit viral replication in honey bee cells in vitro; studies are ongoing. Key outcomes: Researchers and beekeepers are starting to understand how propolis improves immune function and disease resistance in honey bee colonies and are beginning to explore ways to encourage colonies to construct a propolis envelope within beekeeping equipment. This is a major change in perception and behavior because beekeepers have long considered propolis a sticky nuisance within bee colonies, and researchers had not understood the importance of the antimicrobial properties to bee health. The findings will reveal novel approaches to promote honey bee health, define at a fundamental level the use of naturally collected compounds in mitigating disease, and potentially reduce unsustainable colony losses nationwide. Objective 2. Major activities; Data collected: We began evaluating colonies from honey bee stocks derived from A. mellifera ligustica and carnica by scoring them for gentleness (scored from most to least gentle during routine management, using a 1-5 scale, at least 5 times the colony is inspected), honey production (kg produced), and wintering survivorship (frames of bees and brood in early spring). From the top scoring colonies, we conducted additional assays in 2018 for three behavioral traits that help bees defend against pathogens and parasites: high propolis collection (quantified using propolis traps), rapid hygienic behavior (quantified using the freeze-killed brood assay), and low Varroa mite population growth over the season (comparing the proportion of mites in worker brood over time). M. Spivak instrumentally inseminated over 50 queen bees raised from the top performing colonies, and we will continue to evaluate and select the top performing colonies in 2019. Results: We published one peer-review article on new chemical assays for hygienic behavior, have another In Press on indicators of queen bee quality, and a review article submitted on Social Medication by Bees. Key outcomes: Selecting new lines of bees for propolis collection, hygienic behavior, and reduced mite population growth should, in the long-term, result in colonies more able to defend themselves against various parasites and pathogens, and should result in beekeepers having to use fewer chemical treatments to keep colonies alive. Objective 3: Major activities completed, Data collected: Katie Lee, PhD student advised by M. Spivak, defended her thesis in December 2018. Her dissertation included a study of the utility of colony assessment metrics collected from commercial beekeeper operations by the Bee Informed Partnership's Tech-Transfer Team in predicting the risk factors associated with colony health and viability. She also examined the factors associated with queen bee failure, a commonly cited cause of colony mortality. Data collected: Twenty-three commercial, migratory beekeeping operations, representing 475 apiaries, were sampled from 2012-2017. All operations placed colonies in Minnesota or North Dakota over the summer months, and moved them either to California or the Deep South over the winter months. For the study on queen bees, one specific sign attributed to queen failure was studied: poor brood pattern. Pairs of colonies with "good" and "poor" brood patterns in commercial beekeeping operations and used standard metrics to assess queen and colony health. Additionally, queens were exchanged between colony pairs (n = 21) to address whether problems with queen bees were due primarily to the queen or to the colony environment. Results: Over all bee-years, 2.5% and 7.3% of sampled commercial beekeeping colonies died in summer and fall, respectively. Apiary-level mortality from spring to fall averaged 10.0% ± 8.2% (± SD, range = 0 - 34.4%). The metrics that were the best predictors of whether a colony would be weak (nonviable) or dead in fall or winter were queen event, high Varroa levels and low frames of bees in summer or fall. Nosema sp. loads were not useful in predicating colony health and survival. Colonies with queen events - an interruption of the presence of a laying queen - were significantly more likely to be weak or dead in fall or winter. Colonies with >1% mites in spring was predictive whether a colony will have ³3% mites in summer, leading to smaller colonies in fall, which were less likely to be viable in winter. Also, colonies with larger adult bee populations in spring and summer were more likely to have higher mite populations in those sampling periods. No queen quality measures were reliably associated with poor-brood colonies. However, the brood patterns of queens originally from poor-brood colonies significantly improved after placement into a good-brood colony after 21 days, suggesting that the colony environment influenced brood pattern more than the queen's egg laying ability. Key outcomes: Simple metrics can be used by beekeepers to inform management decisions of operations that spend summer months in the Upper Midwest, with the goal of lowering the number of nonviable colonies and decrease the amount of time and effort put into colonies that are likely to fail. The results of the queen study challenges the assumption that brood pattern alone is sufficient to judge queen quality, and emphasize the challenges in determining the root source for problems related to the queen when assessing honey bee colony health.

Publications

  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Wagoner K, Spivak M, Rueppell O. 2018. Brood affects hygienic behavior in the honey bee (Hymenoptera: Apidae). J. Econ. Entomol. toy266, https://doi.org/10.1093/jee/toy266
  • Type: Journal Articles Status: Submitted Year Published: 2019 Citation: Spivak M, Goblirsch, M, Simone-Finstrom M. Social-medication in bees: The line between individual and social regulation. Submitted Curr. Opinion Insect Science.
  • Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Lee, KV, Goblirsch M, McDermott E, Tarpy DR, Spivak M. 2019. Is the brood patterns within a honey bee colony a reliable indicator of queen quality? Insects In Press.
  • Type: Other Status: Published Year Published: 2018 Citation: Spivak M, Koch R, Cira T. 2018. Lets see it from both sides: Perspectives of farmers and commercial beekeeper on protection of honey bees. University of Minnesota Extension. www.beelab.umn.edu/sites/beelab.umn.edu/files/both_sides_web_final.pdf
  • Type: Other Status: Published Year Published: 2018 Citation: Spivak M, Koch R, Cira T. 2018. Getting to know commercial beekeepers. University of Minnesota Extension. www.beelab.umn.edu/sites/beelab.umn.edu/files/web_commercial_beekeepers.pdf


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

Outputs
Target Audience:Target audiences arebeekeepers (backyard, small scale and large scale commercial), and bee breeders to help improve bee health. Other audiences include researchers and other academics, the public, and policy makersinterested in improving flowering landscapes to provide nutritional resources for bee health. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?This research is providing training for three graduate students (K. Lee, M. Shanahan, H. Dalenberg), three undergraduates, and two post-doctoral researchers (M. Goblirsch, and M. Wilson). In addition, two Tech Transfer Team members are employed to survey honey bee colonies in commercial apiaries. Five full or part time people are employed through the Bee Squad program to assist backyard beekeepers in the Twin Cities area. How have the results been disseminated to communities of interest?Peer reviewed research publications, extension publications, web-based materials, videos, books, talks at local, regional, national and international conferences and seminars, and one-on-one training to beekeepers in the field. What do you plan to do during the next reporting period to accomplish the goals?Objective 1 will be changed slightly, due to receiving new funding from USDA-NIFA to explore new ideas. Rather than focusing on how bee select resins, we will focus on the mode of action of the pharmacological properties of resin on honey bee immune function and pathogen defense. We have recently initiated new lab studies to determine the role of propolis volatiles, and bees' contact with propolis in the nest, on modulating honey bee immune response and pathogen defense. Objective 2 and 3 will not be changed.

Impacts
What was accomplished under these goals? Impact The main goal of this project is to improve the health and management practices of honey bee colonies, and to ensure the research results are effectively translated to beekeepers, growers of bee-pollinated crops, and the public. Since 2006, an average of 35% of all honey bee colonies die across the nation from multiple and interacting causes, including pathogens, parasites, pesticides and poor nutrition due to lack of floral resources. In Minnesota, the average mortality of colonies from in 2014-2015 reached a record high of 51%. It is critical to restore honey bee health and economic vitality to the beekeeping industry. Using novel approaches, we will explore honey bees' natural defenses against parasites and diseases, breed bees to enhance these traits, and develop ways to improve the overall management practices of honey bee colonies. Objective 1. Major activities completed / experiments conducted: We published four peer-review articles, one a review article, on the benefits of propolis to honey bee health. The review compiled recent research concerning the behavior of bees in relation to resins and propolis, focusing more on the bees themselves and the potential evolutionary benefits of resin collection. M. Spivak presented these findings at over 20 scientific and beekeeping conferences. Researchers and beekeepers are starting to understand how propolis improves immune function and disease resistance in honey bee colonies and are beginning to explore ways to encourage colonies to construct a propolis envelope within beekeeping equipment. This is a major change in perception and behavior because beekeepers have long considered propolis a sticky nuisance within bee colonies, and researchers had not understood the importance of the antimicrobial properties to bee health. Data collected: This objective will be changed slightly, due to receiving new funding from USDA-NIFA to explore new ideas. Rather than focusing on how bee select resins, we will focus on the mode of action of the pharmacological properties of resin on honey bee immune function and pathogen defense. We have recently initiated new lab studies to determine the role of propolis volatiles, and bees' contact with propolis in the nest, on modulating honey bee immune response and pathogen defense. Summary statistics and discussion of results: We are working on methods for exposing honey bee to propolis volatiles in cages held in incubator, and have no results at this time. Key outcomes or other accomplishments realized: The findings will reveal novel approaches to promote honey bee health, define at a fundamental level the use of naturally collected compounds in mitigating disease, and potentially reduce unsustainable colony losses nationwide. Objective 2. Major activities completed / experiments conducted: We are currently evaluating colonies from diverse honey bee stocks (mixtures of beekeeping stocks derived from A. mellifera ligustica, carnica and caucasica; Italian, Carniolan and Caucasian bees respectively) in MN and LA. Data collected: Beginning in spring 2018, we will evaluate each colony for gentleness (scored from most to least gentle during routine management, using a 1-5 scale, at least 5 times the colony is inspected), honey production (kg produced), wintering survivorship (frames of bees and brood in early spring) for at least 100 colonies from these diverse stocks. We will conduct additional assays for three behavioral traits with the following protocols using gentle colonies that produce the most honey and survive winter well. Key outcomes or other accomplishments realized: Selecting new lines of bees for propolis collection, hygienic behavior, and reduced mite population growth should, in the long-term, result in colonies more able to defend themselves against various parasites and pathogens, and should result in beekeepers having to use fewer chemical treatments to keep colonies alive. Objective 3: Major activities completed / experiments conducted: Outreach is the foundation of the Tech-Transfer Team program for commercial beekeepers. The Tech-Team acts as a liaison between academic and commercial beekeeping communities. Beekeepers have an opportunity to ask questions about research, treatment options, current disease outbreaks, and observable trends. In turn, the data Tech-Teams collect are put into the BIP database anonymously, where they contribute to scientific knowledge. The Tech-Team ensures important findings are easily accessible to beekeepers through posts on the BIP website, presentations at commercial beekeeping conferences, and by communicating directly with commercial beekeepers. A Varroa mite testing kit was developed to assist backyard beekeepers assess the levels of this parasitic mite in their bee colonies. The Mite Kit is being sold at Mann Lake LTD, beekeeping supply company out of Hackensack, MN; at the UMN bookstore, and on our web site (www.beelab.umn.edu). Treatment guidelines for the Varroa mites were updated and published in our University of Minnesota Honey Bees Diseases and Pests manual (available at www.BeeLab.umn.edu) and in the University of Minnesota Bee Squad bulletin sent to Bee Squad customers in the Twin Cities area. Best Management practices for beekeepers are being developed nationally. Data collected: Through the Tech-Transfer Team Program, currently funded through Bee Informed Partnership (BIP: BeeInformed.org) monitored the health of honey bee colonies in 20 commercial beekeepers' operations that own approximately 210,000 colonies, located in ND and MN (migratory bee breeders that move their bees to southern states during winter for queen production). The MN-ND Tech-Transfer Team sampled over 3000 colonies in 2017 to determine levels of pathogen and pests, and the degree of hygienic behavior displayed by the colonies (hygienic behavior is a trait that helps bees resist brood diseases and the parasite mite, Varroa destructor). There are five other Tech Teams in different parts of the U.S. monitor health in approximately 50 other beekeeping operations (over 750,000 colonies). Summary statistics and discussion of results. PhD student, K. Lee, is analyzing the data collected by the TTTs to help define baselines for the parasitic miteVarroa destructorand the parasitic gut fungusNosemaspp. levels in commercial operations in different regions of the US, and to identify risk factors important to those beekeepers. She also is determining the most effective times for commercial beekeepers in the upper Midwest to treat for the parasitic miteVarroa destructorthat leads to lower over-summer and over-winter mortality. Key outcomes or other accomplishments realized: Working with large-scale bee breeders to help them select for both hygienic behavior and propolis collection will impact all US beekeepers that purchase genetic stock (queen bees) from these producers. In turn, this work will benefit the nation through increasing the number of colonies available for pollination and queen production, and reducing the spread of diseases and parasites through implementation of best management practices.

Publications

  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Borba RS, Spivak M. 2017. Propolis envelope in Apis mellifera colonies supports honey bees against the pathogen, Paenibacillus larvae. Sci. Reports 7:11429. DOI:10.1038/s41598-017-11689-w
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Spivak, M, Browning Z, Goblirsch M, Lee K, Otto C, Smart M, Wu-Smart J. 2017. Why does bee health matter? The science surrounding honey bee health concerns and what we can do about it. Council for Agricultural Science and Technology (CAST) Commentary, QTA2017. CAST, Ames, Iowa.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Simone-Finstrom M, Borba RS, Wilson M, Spivak M. 2017 Propolis counteracts some threats to honey bee health. Review. Insects 8: 46: DOI:10.3390/insects8020046
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Wilson MB, Pawlus AD, Brinkman D, Gardner G, Hegeman AD, Spivak M, Cohen JD. 2017. 3-acyl dihydroflavonols from poplar resins collected by honey bees are active against the bee pathogens Paenibacillus larvae and Ascosphaera apis. Phytochemistry 138: 83-92.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Bankova V, Bertelli D, Borba R, Conti BJ, da Silva Cunha IB, Danert C, Eberlin MN , Falcao SI, Isla MI, Moreno MIN, Papotti G, Popova M, Santiago KB, Salas, A, Sawaya ACHF, Schwab NV, Sforcin JM, Simone-Finstrom M, Spivak M, Trusheva B, Vilas-Boas M, Wilson M. Zampini C. 2016. Standard methods for Apis mellifera propolis research. J. Apicul. Res. DOI: 10.1080/00218839.2016.1222661