Source: OHIO STATE UNIVERSITY submitted to
DEVELOPING AND DEPLOYING NOVEL TOOLS TO SUPPORT VARROA MITE IPM FOR ENHANCING HONEY BEE HEALTH FOR POLLINATING SPECIALTY CROPS
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
ACTIVE
Funding Source
OTHER GRANTS
Reporting Frequency
Annual
Accession No.
1031553
Grant No.
2023-51181-41246
Cumulative Award Amt.
$3,942,159.00
Proposal No.
2023-05681
Multistate No.
(N/A)
Project Start Date
Sep 15, 2023
Project End Date
Sep 14, 2027
Grant Year
2023
Program Code
[SCRI]- Specialty Crop Research Initiative
Recipient Organization
OHIO STATE UNIVERSITY
1680 MADISON AVENUE
WOOSTER,OH 44691
Performing Department
(N/A)
Non Technical Summary
There are many stressors contributing to poor health in honey bee colonies that are used for pollination of almonds, apples, blueberries, pumpkins and many other healthy foods. However, the varroa mite, a devastating parasite of honey bees, is consistently identified as the most serious threat to honey bees. Many commercial beekeepers providing hives for crop pollination are struggling to manage varroa as this pest has evolved resistance to common control methods. Despite the challenges, some beekeepers have been successful at using a range of genetic, cultural and chemical varroa control tactics in an Integrated Pest Management approach. Widespread adoption of these practices across commercial beekeeping has been limited by barriers to communication driven by a lack of objective data on the efficacy and timing of varroa control methods and an accounting of the economic costs. Even among beekeepers that are successfully managing varroa today, new approaches for varroa control are badly needed to handle future varroa outbreaks.To reduce honey bee colony losses and maximize the strength of colonies available for crop pollination beekeepers need (1) a re-evaluation of the efficacy and economics of using various combinations of currently available varroa management tools, (2) development of new chemical controls that overcome resistance, and (3) integration and implementation of all approaches into comprehensive varroa management plans.
Animal Health Component
60%
Research Effort Categories
Basic
20%
Applied
60%
Developmental
20%
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
2111212113020%
2163010113080%
Knowledge Area
211 - Insects, Mites, and Other Arthropods Affecting Plants; 216 - Integrated Pest Management Systems;

Subject Of Investigation
1212 - Almond; 3010 - Honey bees;

Field Of Science
1130 - Entomology and acarology;
Goals / Objectives
The sustainability of the pollination-dependent U.S. specialty crop industry, including almonds, blueberries, cranberries, strawberries, apples, cucurbits, melons, vegetable seed and others, depends on a predictable and healthy supply of honey bee colonies. Beekeepers must effectively manage parasitic varroa mite populations to maintain a sufficient number of strong healthy colonies to meet pollination needs. Beekeepers will be required to change the way mites are managed due to growing resistance to widely used miticides. This can be accomplished through a trans-disciplinary approach working with beekeepers to (1) Identify and disseminate cost-effective approaches to mite management using currently available methods and (2) Developing new chemical varroa controls, with new modes of action, combined with optimized use of existing chemical tools, to manage varroa resistance and integrate with existing mite management programs.Social Science Research Objective: A: Identify varroa management programs implemented by beekeepers leading to reduced colony loss, and evaluate beekeeper information-seeking behavior and motivations when managing for varroa.Hypotheses:(1) Common elements of varroa control programs that are related to reduced colony losses will be identified through structured interviews with beekeepers and field testing of management efficacy and varroa resistance(2) Common elements of beekeeper learning and decision-making processes related to varroa control, including economic constraints and source of management guidance, will be identified.Natural Science Research Objective:B: Determine prevalence and mechanisms of varroa resistance to miticides and develop novel resistance-breaking tools for effectively controlling varroa mites in honey bee colonies.Hypotheses:(1) Miticide resistance monitoring will establish that currently registered miticides have reduced effectiveness at controlling varroa populations,(2) Existing pesticides with current registration for other uses and natural products will be safe and effective against varroa resistant to existing miticides and can be formulated for varroa control(3) Efficacy of oxalic acid, a currently registered miticide with no known varroa resistance, can be maximized through improved timing and delivery.Outreach Objective:C: Disseminate best practices for varroa IPM that are cost effective and overcome identified barriers to adoption and reduce colony losses.Hypothesis:Beekeepers will exhibit behavior change and adopt IPM-based varroa control programs if they are demonstrated to be (1) effective at reducing colony losses, (2) economically reasonable, (3) presented by trusted beekeepers or through other trusted sources, and (4) can be tailored to their specific needs.
Project Methods
Social Science EffortsOnline and in-person surveys: Surveys will be conducted at national and regional beekeeping conferences using to explore information-seeking behavior among beekeepers, to assess commonly employed varroa management techniques and to assess the decision making process beekeepers practice concerning varroa management. Semi-structured interviews will be conducted with large-scale beekeepers to gather information on the same topics, but with additional questions . Human ethics (IRB) approval will be obtained by the appropriate institutions before conducting any research with participants.Cost-return studies: Economic costs of the various varroa control methods will be separated into operating and investment costs. Economic benefits from varroa management strategies will be measured in terms of decreased colony mortality at points throughout the year. Lower colony loss rates depending on time of year will result in higher pollination income or honey production. Economic benefits will also be measured for almond producers. Decreased colony mortality will lead to lower risk of inadequate pollination, which should lead to decreasing pollination fees over time. Additionally, growers optimize the number of hives per acre and colony strength to save on input costs. These benefits will be quantified using pollination fee estimatesalong with colony strength and mortality measurements.Natural Science EffortsDirect assessment of colony health: On-the-ground follow ups with beekeepers participating in the semi-structured interviews will directly assess colony health, varroa infestation levels and resistance to current miticides will be conducted. A standard inspection will be conducted in spring, while colonies are pollinating almonds, and in fall, when varroa infestations peak. Canonical correlation analysis will be used to associate monitoring and management practices to a series of beekeepers determinants using CCA. Mortality data will be modeled using a mixed effect GLMM to estimate the relative risk of practices while accounting for confounding factors such as operation size, migratory status and region.Resistance monitoring assays: This cage bioassay method measures the number of varroa dislodged from bees when exposed to a small strip of Apivar® (amitraz) in a 1-quart plastic container to assess amitraz resistance. Resistance monitoring tests will be conducted with the same beekeepers in multiple years so that changes in amitraz resistance levels can be documented over time.Miticide use patterns: A 10-gram sample of wax from the center of 2 brood combs in colonies in each of 25 apiaries will be collected from colonies subject to resistance monitoring assays. Wax samples will be pooled at the apiary level and miticide concentrations will be determined by GC-MS or LC-MS at the USDA-AMS laboratory in Gastonia NC. Miticide use patterns will be paired to results of resistance testing and miticide concentrations in wax to determine mite control methods associated with the development of resistance.Screening novel miticides: Potential miticide compounds will be screened for varroa toxicity and bee safety first by generating separate dose-response curves using vial bioassays. A decision tree will be used to evaluate results and promote promising compounds to cage testing wher the number of varroa that fall through the mesh flooring of the cages during the 48 hour trial will be counted and removed then the bees will be subjected to an alcohol wash to remove remaining varroa. Survivorship data will be analyzed using binomial-logit generalized linear mixed-effects models (GLMMs) to establish dose-mortality curves.Field testing varroacide formulations: Mini-nucleus colonies will be prepared for testing 3 concentrations/product. Each concentration will have 3 replicates (2 modified brood boxes). A negative control and positive control will be included. The efficacy of mite-kill (%) will be calculated based on comparing the infestation percentage at day 15 and day 28 to the percentage of infestation at day 0. Data will be analyzed using a mixed model ANOVA. This preliminary analysis will then inform the concentration or dosage of formulations taken to full field trials.For each field trial colony assessments and varroa population estimates will be made before initiation of the trial, at the end, and at least two times while the miticide application is present. Analysis of all field data will utilize a GLMM-framework. At least 10 g of honey and wax will each be collected from 5 randomly selected colonies in the treatment and control groups for pesticide residue testing at the USDA-AMS lab in Gastonia, NC.Optimization of oxalic acid as a miticide: Field trial involving full-sized colonies will test temperature of oxalic acid vaporization (160°C, 180°C, 210°C, and 230°C), seasonal differences in oxalic acid efficacy, and five different common application methods used by beekeepers to apply OA to their colonies. Varroa infestation and colony strength parameters will be measured.Outreach effortsDemonstration trials: Three demonstration trials will be performed by Bee Informed Partnership Tech Team Specialists using beekeeper-managed colonies. Standard colony health data will be collected, including varroa levels by alcohol wash. One treatment group will serve as a positive control, managed according to the participating beekeeper's standard varroa management scheme and compare with demonstrated successful practices identified through the work of the project, either existing methods proven successful by beekeepers or novel miticides will be used. Bee Informed Partnership Tech Teams will monitor colonies prior to specialty crop pollination events.Case studies: Narrative case studies will be developed using information initially collected through semi-structured interviews, decision making assessment, and on-the-ground follow-ups above. Beekeeper permission to be included in publicly available case studies will be sought, and additional documentation of IPM treatment regimes by the beekeepers will be established. Cost analysis of varroa control will be included.Varroa Management Decision Support Tools and Resources: The Varroa Decision Support Tool will be adapted for large-scale beekeepers by expanding the decision criteria to include the treatment windows based on their business model and the cost and return information. The tool will be presented in the form of an interactive Excel spreadsheet that will allow beekeepers to input information corresponding to the specifics of their operation and to make decisions.Evaluation:Major Indicators(1) Number of beekeepers reached(2)Number of novel miticides identified(3)Number of existing successful tools identified(4)Increase in knowledge & intention to change behavior(5)Adoption of recommended best practices(6)Decrease in varroa parasitism and increase in honey bee colony healthEvidence for(1)Beekeeper support, new stakeholders(2)Successful decision tool and varroa miticide pipeline(3)Successful cooperation with stakeholders(4)Access to effectively communicated information appropriate for real-world scenarios(5)Use of information, or immediate corrective action after pest management recommendation(6)Adequate training programsEvaluation type(1)Quantitative(2)Quantitative(3)Quantitative / qualitative(4)Quantitative(5)Quantitative / qualitative(6)Quantitative / qualitativeEvaluation Methods(1)Analytics for website hits and Podcast listens, submitted questionnaires(2)Lab and field trial data(3)Interviews, Demonstration Trial data, BIP Tech Team colony health/productivity monitoring(4)Pre-/post- questionnaires, interviews, BIP Survey(5)Pre-/post- questionnaires, interviews, BIP Survey(6)Pre-/post- questionnaires, interviews, BIP Tech Team health/productivity monitoring, BIP Survey

Progress 09/15/23 to 09/14/24

Outputs
Target Audience:Over 5500 beekeepers and other stakeholders received60oral presentations made in 18 states by members of the team on varroa mite control in honey bee colonies.Topics included the basics of mite control andmore specialized presentations on pesticide regulation, miticide resistance and improved mite control approaches. Beekeepers at all levels, from hobbyist to commercial, are the primary target audience for these communication activities as all beekeepers continue to struggle with effective varroa mite management. Other target audiences reached includeveterinarians incorporating bee health into their practice and state-level pesticide control officials responsible for enforcing pesticide law. Changes/Problems:The dissolution of one of the project partners, the Bee Informed Partnership (BIP) resulted in the removal of Steinhauer and Fauvel from the project. Most work to be performed by BIP under these objectives have been taken up by other team members. The national beekeeper survey (Obj. A2) incorporating questions on Varroa management is being conducted by Williams (Auburn) and partners. Promotion of this survey is being coordinated by the Mullica and the HBHC. Coordination with beekeepers to identify amitraz resistant Varroa mites and collect wax samples for miticide residue analysis (Obj. B2) will be conducted by Rinkevich (USDA-ARS, Baton Rouge) who is developing miticide resistance assays and has many collaborations with commercial beekeepers throughout the US. The team has not yet identified a way to conduct demonstration trials (Obj. C1) in Year 3 and 4 without the assistance of the BIP Tech Teams. The beekeeping cost and returns study was delayed due to Goodrich's transition from UC Davis to the University of Illinois at Urbana-Champaign. However, Goodrich will have a Master's student fully funded by this project in the spring of 2025 to begin interviews and working on the study. What opportunities for training and professional development has the project provided?Five postdoctoral researchers or staff scientists led components of the field miticide testing and gained experience in leading research teams. Ten graduate students, both M.S. and Ph.D.were trained in the work of testing miticides in laboratory or field settings. Components of this research will appear in their dissertations or theses. Eleven undergraduate students assisted with miticide research. Two of these students presented their work at the Annual Meeting of the Entomological Society of America in Maryland in November 2023 and five students presented to bee scientists and beekeepers at the American Bee Research Conference in New Orleans in January 2024. How have the results been disseminated to communities of interest?Mulica (HBHC) released an updated list of approved bee medications for US and Canadian beekeepers in April 2024 and was downloaded 40 times. The Honey Bee Health Coalition Tools for Varroa Management Guide was downloaded approximately 8000 times from Sept. 2023-Aug. 2024 (Obj. C3). Work informed by the work of this project was used to train of veterinarians through the 2024 Honey Bee Veterinary Consortium meeting where Bartlett and Tokach (Ph.D. Student at Auburn). State apiary inspectors and state pesticide control personnel were informed about miticide use and varroa resistance by Johnson at the Pesticide Inspector Residential Training Program in North Carolina in July. Additionally, members of the project presented work to over 5500 beekeepers at at over 40 beekeeper conferences and meetings at local, regional and national levels. Members of this project (Bartlett and Shannon [Ph.D. student at Ohio]) were also featured on the popular "Two Bees in a Podcast" out of the University of Florida. Work under Objective A will identify beekeepers' preferred means of learning and, following interviews conducted in 2024 and 2025, we will prioritize and develop dissemination methods using the media beekeepers identify as preferred. What do you plan to do during the next reporting period to accomplish the goals?Beekeepers participating in Rinkevich's resistance monitoring and wax sampling work (Obj. B1-2) will be interviewed using the survey developed by Ballen and Williams to both determine how beekeepers prefer to gain new information about beekeeping and varroa mites as well as an assessment of their current mite control practices (Obj. A1-3). Goodrich will contact these and other beekeepers to conduct interviews to determine the cost-return of beekeepers and assess the financial impact of varroa (Obj. A4). Varroa management questions will again appear in the US Beekeeping survey conducted by Williams and team to allow assessment of stakeholder behavior change over the course of the project (Obj. C5). New miticides suggested by colleagues in industry and other sources will continue to be explored using lab assays (Obj B3.1 and B3.2) Jack (Florida) will test carbamate compounds. Among the potential miticidal compounds tested under Obj, B, Beauvaria bassiana shows the most promise and will be tested in field trials in 2025 by Johnson (Ohio) and Cook (USDA-ARS Beltsville). Nasr (Saskatchewan) will test miticide active ingredients with existing registration for non-bee uses in a low-density plastic formulation (Obj. B3.3). Oxalic acid is already registered and is currently the most important alternative to the failing miticide amitraz. Jack (Florida), Nasr (Saskatchewan), Williams (Auburn) and Bartlett (Georgia) will continue to evaluate the efficacy of different oxalic acid delivery methods (vaporization temperature) and formulations (Varroxsan, OA+glycerin) (Obj. B4). Varroa Management Decision Support Tools managed by Mulica and the Honey Bee Health Coalition will be updated to incorporate findings on oxalic acid delivery methods and formulations (Obj. C3). Additional communication through methods identified in beekeeper interviews (e.g. podcasts or short form video) will also be developed to promote communication of the Best Management Practices identified by team members and other researchers (Obj. C2)

Impacts
What was accomplished under these goals? Social Science and Outreach Objectives (A and C) Williams (Auburn) conducted the 2023-2024 US Beekeeping survey of annual honey bee colony losses, which includes questions related to effective varroa management. Mulica (HBHC) assisted in contacting beekeeper participants and promoting this survey (Obj. A2). This broad online survey of beekeepers includes questions on varroa management that will form the baseline against which to compare beekeeper knowledge gains and behavior changes (Obj. C5). Ballen and Williams (Auburn) have developed and modified a questionnaire that addresses the following: (1) obtains basic demographic information about beekeepers such as their age and reason for keeping bees, (2) their perceptions of the threat of varroa, (3) how they treat varroa annually, (4) their limitations to treating varroa with specific methods, (5) how they monitor their treatments, (6) where they obtain sources of information for varroa treatment, (7) how they prefer to receive information. This survey has been submitted to the Institutional Review Board and should gain an exemption allowing surveys to be conducted Natural Science Objectives (B) Rinkevich (USDA-ARS, Baton Rouge) conducted miticide bioassays with fluvalinate and coumaphos to establish baseline LC50 for a miticide susceptible population. Resistance tests with Apistan (fluvalinate) were completed at different temperatures and surface area of Apistan strips in the container tests. Results showed there was no significant effect of temperature or surface area size on the efficacy of Apistan, but the test population demonstrated some resistance to this compound. CheckMite (coumaphos) tests have not been possible as this product is no longer available. Development of resistance monitoring tests for oxalic acid has been unsuccessful as Aluen CAP causes few mites to drop in cage tests -- this test will need to be redesigned for longer exposure periods or higher concentrations of oxalic acid (Obj. B1). Beekeepers have provided Varroa mites and wax samples from 60 apiaries for genotyping and pesticide testing to Rinkevich. Varroa from 26 samples have been genotyped and they have high levels of amitraz resistance genetics (92% avg, 53-100%). This is concerning as resistance is being observed in operations that have never used amitraz. Miticide residue analysis of all 60 wax samples is being conducted by Roger Simmonds at USDA-AMS in Gastonia, NC (Obj. B2). Cook (USDA-ARS Beltsville), Bartlett (Georgia) and Johnson (Ohio) conducted laboratory trials to identify new miticides using spray adjuvant constituents, including ethoxylates and organosilicones, falcarinol, several plant extracts, organic acids and the entomopathogenic fungus Beauvaria basssiana (Obj. B3.1 and B3.2). Field testing by Johnson indicated that a novel extended release oxalic acid formulation incorporating an adjuvant was more effective than oxalic acid alone (Obj. B3.3). This formulation was patented by OSU and licensed to the an existing registrant for oxalic acid, Chemicals Laif, and may incorporated into a commercially available for beekeepers. Nasr (Saskatchewan) field tested two active ingredients that are registered as miticides for non-beekeeping uses in small experimental colonies. A bee-safe and effective dose for these compounds was identified (Obj B3.3). Jack (Florida) performed experiments and published an article comparing the efficacy of oxalic acid vaporization, fogging and dribble (Obj. B4.3). Efficacy of the only currently available extended release oxalic acid product, Varroxsan, was compared with a new registered amitraz formulation, Amiflex, in 65 full-sized colonies in a Southern climate by Bartlett (Georgia) and Williams (Auburn). The efficacy and colony-level effects of Varroxsan at different doses (½-1 ½) was tested in a Northern climate by Nasr (Saskatchewan). Nasr also tested the efficacy of using repeated vaporization of oxalic acid to control varroa (Obj. B4) along with characterizing the distribution of oxalic acid vapor within the colony (Obj. B4.2).

Publications

  • Type: Peer Reviewed Journal Articles Status: Published Year Published: 2023 Citation: Lewis J Bartlett, Christian Baker, Selina Bruckner, Keith S Delaplane, Ethan J Hackmeyer, Chama Phankaew, Geoffrey R Williams, Jennifer A Berry, No evidence to support the use of glyceroloxalic acid mixtures delivered via paper towel for controlling Varroa destructor (Mesostigmata: Varroidae) mites in the Southeast United States, Journal of Insect Science, Volume 23, Issue 6, November 2023.
  • Type: Peer Reviewed Journal Articles Status: Published Year Published: 2024 Citation: Lewis J Bartlett, Michael Boots, Berry J Brosi, Keith S Delaplane, Travis L Dynes, Jacobus C de Roode, Faster-growing parasites threaten host populations via patch-level population dynamics and higher virulence; a case study in Varroa mites (Mesostigmata: Varroidae) and honey bees (Hymenoptera: Apidae), Journal of Insect Science, Volume 24, Issue 3, May 2024.
  • Type: Peer Reviewed Journal Articles Status: Published Year Published: 2023 Citation: Jennifer A Berry, S Kris Braman, Keith S Delaplane, Lewis J Bartlett, Inducing a summer brood break increases the efficacy of oxalic acid vaporization for Varroa destructor (Mesostigmata: Varroidae) control in Apis mellifera (Hymenoptera: Apidae) colonies, Journal of Insect Science, Volume 23, Issue 6, November 2023.
  • Type: Peer Reviewed Journal Articles Status: Published Year Published: 2023 Citation: Cody Prouty, Hossam F Abou-Shaara, Branden Stanford, James D Ellis, Cameron Jack, Oxalic acid application method and treatment intervals for reduction of Varroa destructor (Mesostigmata: Varroidae) populations in Apis mellifera (Hymenoptera: Apidae) colonies, Journal of Insect Science, Volume 23, Issue 6, November 2023.
  • Type: Peer Reviewed Journal Articles Status: Published Year Published: 2024 Citation: Cameron J Jack, Humberto Boncristiani, Cody Prouty, Daniel R Schmehl, James D Ellis, Evaluating the seasonal efficacy of commonly used chemical treatments on Varroa destructor (Mesostigmata: Varroidae) population resurgence in honey bee colonies, Journal of Insect Science, Volume 24, Issue 3, May 2024.
  • Type: Peer Reviewed Journal Articles Status: Published Year Published: 2024 Citation: Cook, S.C., Johnson, J.D., Rogers, C.W., Sachs, I.E., Feng, X., Plettner, E. The efficacy of 1-allyloxy-4-propoxybenzene against Varroa destructor mites in honey bee colonies from Maryland, USA. J. Ins. Sci., 24(3): 9
  • Type: Peer Reviewed Journal Articles Status: Published Year Published: 2023 Citation: Shannon B, Jeon H, Johnson RM. 2023. Review: the risks of spray adjuvants to honey bees. J. Insect Sci. 23(6).
  • Type: Peer Reviewed Journal Articles Status: Published Year Published: 2024 Citation: Frank D Rinkevich, Robert G Danka, Thomas E Rinderer, Joseph W Margotta, Lewis J Bartlett, Kristen B Healy, Relative impacts of Varroa destructor (Mesostigmata:Varroidae) infestation and pesticide exposure on honey bee colony health and survival in a high-intensity corn and soybean producing region in northern Iowa, Journal of Insect Science, Volume 24, Issue 3, May 2024
  • Type: Peer Reviewed Journal Articles Status: Published Year Published: 2024 Citation: Lewis J Bartlett, Suleyman Alparslan, Selina Bruckner, Deborah A Delaney, John F Menz, Geoffrey R Williams, Keith S Delaplane, Neonicotinoid exposure increases Varroa destructor (Mesostigmata: Varroidae) mite parasitism severity in honey bee colonies and is not mitigated by increased colony genetic diversity, Journal of Insect Science, Volume 24, Issue 3, May 2024,