NC_old1173: Sustainable Solutions to Problems Affecting Bee Health

(Multistate Research Project)

Status: Inactive/Terminating

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Annual/Termination Reports:

[02/27/2020] [02/05/2021] [02/23/2022] [03/01/2023] [02/28/2023]

Date of Annual Report: 02/27/2020

Report Information

Annual Meeting Dates: 01/09/2020 - 01/09/2020
Period the Report Covers: 02/02/2019 - 01/01/2020

Participants

Brief Summary of Minutes

Please see attachement below for NC1173's 2019 annual report.

Minutes Attachment:

NC1173 Annual Report 2020_worddoc_FINAL.pdf

Accomplishments

Publications

Impact Statements

Date of Annual Report: 02/05/2021

Report Information

Annual Meeting Dates: 01/08/2021 - 01/08/2021
Period the Report Covers: 01/01/2020 - 12/31/2020

Participants

Participants Attachment:

NC1173 Partcipant List Jan 2021.jpg

Brief Summary of Minutes

Brief Summary of Annual NC1173 Multi-State Project Meeting

Minutes taken by Michelle Flenniken (Montana State University), Judy Wu-Smart (University of Nebraska, and Margarita Lopez-Uribe (Penn State)

The NC1173 business meeting was conducted as part of the 2021 American Bee Research Conference (ABRC) with the American Association of Professional Apiculturists (AAPA) meeting via Zoom due to the SARS-CoV-2 pandemic. The ABRC was held for two days (Jan 7-8, 2021) and serves as the scientific program for the NC1173 multi-state group. An agenda for the ABRC meeting is online (https://aapa.cyberbee.net/wp-content/uploads/2021/01/2021_ABRC_Schedule_Final-downloaded-Jan5_2021-1.pdf), was submitted in conjunction with this report, and proceedings will be published in the coming months.

The business meeting was called to order at 10:00 AM by chairperson Dr. Michelle Flenniken from Montana State University. Attendance was recorded via zoom login information. Dr. Michelle Flenniken reviewed the current status of the multi-state project. She reported that there are currently 37 members listed in NIMMS (27 of whom were in attendance) representing 26 institutions. Dr. Michelle Flenniken reminded members to submit their publications, activities, and milestones, so that these efforts may be reported in the 2021 NC1173 report due within 60 days of the mee ting.

Dr. Erica Kistner-Thomas provided an update on USDA-NIFA-AFRI opportunities. She reported that since their move to Kansas City, Missouri, they have hired many new people after a dramatic loss in staff (i.e., ~ 80%). The ~128 new hires included 18 new national program leaders, including herself, Megan O'Rouke may also be another good contact for this group. In 2020 there were 61 applications submitted to the Pollinator Health Program and funded 11 projects. The 2021 budget is similar therefore she expects a similar number of projects will be funded. Dr. Erica Kistner-Thomas encouraged new faculty members who have not yet received a USDA-funded research grant and with less than 5-years of experience to apply for the “new-investigator” opportunity, with a funding level of $300,000 for up to 2-years. In 2021, she noted that the maximum requires for “standard USDA grants was raised to $750,000 and the deadline for submission is May 27, 2021 at 5 pm EST (see: https://nifa.usda.gov/funding-opportunity/agriculture-and-food-research-initiative-foundational-applied-science-program). Members can contact her directly with questions (i.e., Dr. Erica Kistner-Thomas, National Program Leader, National Institute of Food and Agriculture, Institute of Food Production and Sustainability, Email: ekistnerthomas@usda.gov).

Dr. Michelle Flenniken reported that the previous NC1173 report, which was submitted by Dr. Judy Wu-Smart, was submitted in 2020 and Project Director William (Bill Barker) highlighted components of that report. Specifically, the success of NC1173 members work together to garner additional funding for research (i.e., FFAR funding awarded for a collaborative effort by Auburn University, University of Nebraska, University of Georgia, and investigators in Spain); IPM research efforts at Iowa State University, University of Nebraska, and Montana State University; and landscape level research, including the BeeScape website developed by investigators at Penn State (https://beescape.org/). He encouraged the team to focus our report to highlight synergistic efforts, including highlighting publications and grants co-authored by NC1173 members across institutions. In addition, he remarked that he liked the use of “bold text” to highlight NC1173 co-authors. Dr. William (Bill) Barker suggested that NC1173 members read the Sand County Almanac by Aldo Leopold and Braving Sweetgrass by Robin Wall Kimmerer and acknowledged that most land grant universities are situated on historical tribal lands. He encouraged members to work with Native Americans / indigenous people, new/beginning farmers, and veterans in our research and outreach projects, as well as consider focusing on large-scale regenerative systems and/or the development of those systems. He noted that Dr. Christina Hamilton, the other NC1173 Administrative Advisor could not join us this year.

Dr. Flenniken reiterated a decision from the 2020 meeting, next meeting will be held in with the American Bee Research Conference, which will be held in conjunction with American Honey Producers Association (AHPA) Meeting, which will be in Baton Rouge, Louisiana at the Crown Plaza Hotel, November 30-December 4, 2021; the specific date and time will be finalized closer to the meeting time. The 2023 NC1173 meeting will be held with the ABRC meeting in conjunction with the American Beekeeping Federation (ABF) in January 2023. Dr. William (Bill) Barker will confirm that the future meeting plans are in line with USDA guidelines, but given the importance of NC1173 members meeting with stakeholder groups, and flexibility due to the pandemic that it is likely that our future meeting plans will be approved. Information on future meetings is provided on the AAPA website (https://aapa.cyberbee.net/abrc-2021/).

The floor was opened for discussion of other business. Dr. Judy Wu-Smart asked the group about their interest in a larger-scale effort to further research problems of pesticide contamination, particularly large-scale contamination as a result of processing chemically treated seeds (as she described during her ABRC/NC1173) presentation. Dr. Juliana Rangel suggested that Dr. Judy Wu-Smart should consider leading an USDA-NIFA-AFRI CAPS Project grant on this topic. Dr. Michelle Flenniken also commented on the importance of this research topic that has important real-world impact for bees and other pollinators.

Dr. Margarita Lopez Uribe announced that she will send an email to see if those who submitted ABRC abstracts would like to publish them in Bee Culture and that authors may opt out of the publication of their abstracts at that time.

Dr. Juliana Rangel asked about the minutes of the 2020 meeting and the election of current officers and Dr. Michelle Flenniken provided the minutes and let the group know that in 2020 she was elected as Chair of NC1173 and Dr. Margarita Lopez-Uribe (Penn State) was elected as vice-chair for 2020-2022. The floor was opened for discussion of other business, but in the absence of additional discussion Dr. Flenniken adjourned the meeting at 10:40 am (EST).

Minutes Attachment:

NC1173 Annual Report 2021_FINAL.docx

Accomplishments

NC1173 Objectives <ol> <li>To evaluate the role, causative mechanisms, and interaction effects of biotic stressors</li> </ol> (i.e., parasitic mites, pests, and pathogens) and abiotic stressors (i.e., exposure to pesticides, poor habitat and nutrition, management practices) on the survival, health and productivity of honey bee colonies as well as within pollinator communities. <ol start="2"> <li>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.</li> </ol> <ol start="3"> <li>To develop and recommend "best management practices" for beekeepers, growers, land managers and homeowners to promote health of honey bees and pollinator communities.</li> </ol> NC1173 Accomplishments:  Objective 1a: (Biotic Stressors: Pests & Pathogens) The Varroa destructor mite is one of the deadliest honey bee pathogens currently facing the US beekeeping industry. Varroa destructor is an ectoparasitic mite that feeds on honey bees and decimates colony populations resulting in colony death. Varroa mites also transmit viruses within and between colonies. High mite infestation coupled with high levels of viruses, including deformed wing virus (DWV), are often associated with overwinter losses of honey bee colonies. NC1173 members are addressing the Varroa destructor mite challenge by developing novel chemical and biological control options for management (Johnson, OSU; Ellis, UF; Shepard, WSU), determining the efficacy of commonly used miticides (Ellis, UF), and examining management practices, including the use of screened bottom boards, that reduce mite populations (Huang, MI State). The Connecticut Agricultural Experiment Station team (Eitzer, Stoner, Cowles are collaborating with Williams (Auburn) and Cook and Evans (USDA) to evaluate Aluen CAP for Varroa mite management. This product is considered organic and will likely be compatible with use during nectar flow. It provides a 42-day continuous exposure of oxalic acid through honey bee interaction with cellulose matrix strips left in the hive draped over brood frames. Aluen CAP is produced by Cooperativo de Trabajo Abicola Pampero (Buenos Aires, Argentina). Both U.S. data and a registration partner will be needed in order to obtain a U.S. EPA registration. These efforts in conjunction with continued investigation of hygienic behavior (Spivak, UM) are aimed at mitigating mite-associated colony losses. NC1173 members are also examining the impact of pathogens on colony health and longevity (almonds-Flenniken, MT State; samples from 2015 US National Honey Bee Disease Survey – Grozinger, PSU). These efforts take into account the relative role of a variety of abiotic and biotic factors, including landscape, chemical exposure, and  inter-bee taxa pathogen transmission with insect communities (Wu-Smart, UNL, Hines, Grozinger, PSU; Flenniken MT State; Tarpy, NCSU; Rangel, TAMU). For example, Hines (PSU) investigated differential microsporidian infection levels by bee species and by habitat and Flenniken (MT State) examined relative prevalence and abundance of a virus in sympatric mining bees and honey bees. As another example, Rangel and collaborators found that ants living in and around honey bee colonies indeed serve as mechanical vectors of several honey bee associated viruses. In addition, the influence of nutrition (specifically phytosterols and protein) on the outcome of pathogenic infections is another area of active research (in orchards-Ramesh OSU, in laboratory-based experiments, Flenniken, MT State, and in honey bees infected with Nosema or DWV, Rangel, TAMU) NC1173 members are also investigating honey bee antiviral defense mechanisms including the heat shock response and dsRNA-triggered virus restriction (Flenniken MT State), and the transcriptional and epigenomic responses that regulate honey bee gene expression in response to IAPV infection (Li-Byarlay, Central State and Tarpy NCSU); Rangel, TAMU. Examining the impact of putative immune stimulants that may reduce virus infection (i.e., fungal extracts and thyme oil) (Sheppard, WSU; Flenniken, MT State), and the role of propolis in promoting colony health (Spivak, UM). The team is also involved in virus discovery and monitoring (Flenniken MT, State; Schroeder UMN; Lopez-Uribe PSU; Grozinger PSU; Tarpy, NCSU). Behavioral responses including hygienic behavior, as well as the potential of social fever, are also under continued investigation (Spivak, UM). Members are also looking at self-removal behavior of workers in response to Varroa parasitization and/or other stressors (Rangel, TAMU). Members of the NC State Apiculture Program investigated vertical transmission viruses and other pathogens from honey bee queens to their offspring (Rueppell & Tarpy, NCSU), the transcriptome and epigenome dynamics of honey bees in response to virus infection (Rueppell & Tarpy, NCSU; Li-Byarlay, CSU), and the horizontal transmission of viruses from workers to queens (Lee, Spivak, Schroeder, UM; Tarpy, NCSU). Short outcomes, Objective 1a: The strong association between Varroa destructor, deformed wing virus (DWV), and high overwintering colony losses (OCL) of honey bees is well established. Research indicates that increasing floral diversity in pollinator habitats reduces pathogen levels (Hines, Grozinger, PSU). Managed bee populations in the US have a greater diversity of viruses than previously realized (Grozinger, PSU) and virus infections at the colony level are dynamic, and thus longitudinal studies that precisely control sampling date are important to understand the impact of pathogens on honey bees at the colony level (Flenniken, MT State). At the molecular level, IAPV-infection causes epigenetic changes (e.g., DNA methylation) in pupae, which impacts gene expression in adult honey bees(Li-Byarlay CSU), and that the heat shock stress response pathway is an important antiviral defense response to a model virus (Flenniken, MT State). Investigators at WSU are breeding a novel strain of Metarhizium fungus for improvement as a biological control agent against Varroa mites (Sheppard, WSU). The team conducted outdoor studies comparing Metarhizium to oxalic acid, a commonly utilized mite treatment, and showed that the Metarhizum exhibited comparable mite control (Sheppard, WSU). Additional testing (i.e., nutritional analysis) of polypore mushroom extracts for potential use as a honey bee feed additive were carried out and indicated that the extracts have a mineral composition similar to honey and pollen and an AAFCO requested longevity study was completed (Sheppard, WSU). WSU has coordinated with AAFCO and the FDA to seek a smooth and quick route to registration as a honey bee feed additive. Outputs Objective 1a: NC1173 published numerous peer-reviewed publications related to pest and pathogen stressors, which are listed at the end of this report; many of them are open-access. A USDA APHIS PPQ grant was secured to continue investigation into landscape factors driving wild bee pathogen levels in another region (North Carolina), which, together with Pennsylvania data, will help refine best management practices for promoting healthy bees (Hines, Grozinger, PSU). Williams (Auburn) found that the parasitic mite Varroa destructor, but not neonicotinoids, negatively affected worker food glands in honey bees. Conversely, drones appeared more sensitive to neonicotinoids, as those exposed to the insecticides exhibited reduced sperm quality. By performing a meta-analysis, antagonistic interactions between pesticides and parasites appear to be overlooked by the scientific community. They also identified alternative food sources for small hive beetle in the SE United States. Objective 1b: (Abiotic Stressors: Pesticides, Forage Availability, Nutrition) Major abiotic stressors contributing to honey bee health decline include pesticide exposure and malnutrition. NC1173 members are addressing these factors through studies examining the pesticide residue levels found in bee forage (floral nectar and pollen) in ornamental plants treated with systemic insecticides (Eitzer, Stoner, and Cowles, The Connecticut Agricultural Experiment Station), examining the pesticide residue levels found in bee forage in urban areas (Rangel, TAMU; Huang, MI State; Ellis, UF), examining the role existing tree lines play as drift barriers to reduce off-target contamination from neonicotinoid-laden dust released during corn planting into forbs growing near corn fields (Wu-Smart, UNL), examining which plants bees are utilizing in natural landscapes and in open spaces near agricultural crops (Kim, Speisman, KSU; Wu-Smart, UNL), and the microbial (bacterial and fungal) communities in bee forage (Danforth, Cornell) to better understand the nutritional requirements of managed and wild bees (Osmia cornifrons (Megachilidae)) and the role fungicides play on these microbes. Further, some of these issues with pesticide exposure, malnutrition, and or pollination deficits/limitations are being examined in specific cropping systems (apples-Danforth, Cornell; black cherry-Hoover & Grozinger, PSU; corn/soybeans-Wu-Smart, UNL). In addition, Ellis and team are working to assess the potential toxicity of pesticides to various honey bee life stages and characterize risks associated with exposure to these compounds (Ellis, UF). Winfree (Rutgers) published the results of a nation-wide study showing that many crops, and especially spring-blooming fruit crops, are pollination-limited in the USA (Reilly et al 2020). Ongoing work includes identification of the main flowering plant species used as pollen sources by spring-flying native bee species such as Andrena and Osmia, which are important pollinators of spring tree fruit (Winfree, Rutgers). Evaluating the nutritional needs of bees to improve planting schemes (Grozinger, Patch, PSU).  NC1173 members evaluated the protein and lipid ratios of pollen of 82 plant species and three bee species, and demonstrated a broad range of ratios, which seem to correspond with different preferences for the different bee species (Vaudo et al 2020). Using DNA barcoding, they found in urban landscapes, honey bees foraging preferences shift throughout the growing season from trees, to weedy plants, to ornamental plant species in the fall (Sponsler et al, 2020a, b). They found significant variation in visitation patterns of pollinators to different annual ornamental plant species and cultivars, and found a significant effect of season, year, and site (Erickson et al, 2020). Developing a National Insecticide Toxic Load Map (Grozinger, PSU).  We published a spatial map of pesticide use patterns across the United States (Douglas et al 2020). Total toxic load of applied insecticides has increased nationally over the last 20 years, with some counties showing increases of over 100-fold.  This map allows stakeholders and policymakers to identify sites to focus alternative management or conservation efforts. Funding was provided by the USDA-NIFA-AFRI, the USDA FFAR, the National Socio-Environmental Synthesis Center. Evaluating the role of landscape and climate on wild bee health (Grozinger, PSU).  To support large-scale studies of the effects of land use, habitat, weather and climate on wild bee species, the PSU team organized, validated, and shared an analysis-ready version of one of the few existing long-term monitoring datasets for wild bees in the United States (Kammerer et al 2020). This work was supported by funding from the USDA-NIFA Postdoctoral training program and the USDA FFAR. In addition, the PSU team secured funding to develop resources to improve pollen diagnostic abilities by developing a streamlined metabarcoding pipeline (Grozinger) and pollen image library (Boyle) (Funding from PA Dept of Agriculture). Efforts by Eitzer, Stoner, Cowles (Conn) include the establishment of high-yielding floral resources plots. These plots will be used to support honey bee genetic improvement programs, and also to enhance landscapes to support a broad diversity of pollinators.  They plan to obtain quantitative data on honey yield from hives using these plots which could spur their acceptance in fixed-land honey crops.  To date 10 of 12 planned species have been established on these plots.  Methods to establish these plants are described in this video:  <a href="https://www.youtube.com/watch?v=rzyEyNf5CaU">https://www.youtube.com/watch?v=rzyEyNf5CaU</a> . NC1173 members in the NC State Apiculture Program investigated the effects of abiotic stressors (temperature and pesticides) on honey bee queens and particularly their reproductive quality (Pettis, Tarpy). They determined the thermal limits to sperm survival in queen spermathecae (sperm storage organs) as well the proteomic changes in queens as a consequence of temperature and pesticide exposures. The team at Michigan State University (Z. Huang Lab) studied the effect of neonictinoids on honey bee mortality at different temperatures and found the toxicity of both imidacloprid and thiamethoxam were more toxic to winter bees (higher mortality) at 25°C compared to 35°C. They also evaluated longevity of caged worker bees after they were fed with different pollen substitutes.  They found that commercial pollen substitutes show large variations in sustaining honey bee longevity. The Connecticut Agricultural Experiment Station team (Eitzer, Stoner, Cowles) collected trapped pollen from honey bee colonies in different environments (ornamental plant nurseries and botanical gardens), and are analyzing the plant sources of the pollen and the pesticide residues found in the pollen. The plant sources were analyzed using palynology (identification of acetolyzed pollen using light microscopy) and by DNA metabarcoding (contracting with researchers at the University of Maine and Ohio State University, respectively). The pesticide residues are extracted using a version of the QuEChERS protocol and then analyzed using liquid chromatography/mass spectrometry (contracting with researchers at Cornell University and the US Department of Agriculture) and gas chromatography and mass spectrometry (US Department of Agriculture). They are comparing the results of the two methods of plant identification and relating the plant sources of the pollen to the pesticide residues found. The Connecticut team is collaborating with Webster at Kentucky State University to measure queen pheromone levels using a new liquid chromatography/high resolution mass spectrometry rather than a derivatization-based GC/MS procedure (Eitzer, Stoner, Cowles). The UNL Bee Lab reported challenges with abnormally high bee losses at a large 93,000 acres research property (Wu-Smart, UNL). Colonies losses were consistent with 0% survivability over multiple years and bees showed signs of acute mortality potentially due to pesticide exposure. In 2019, UNL shifted research focuses to specifically investigate and examine these bee losses using the “Dead Bee Trap Monitoring Study” and this year they identified a potential connection between observed bee losses to pesticide contamination problems originating from an ethanol plant just north of the property. As a result of our research, we have discovered a novel practice of “disposing” surplus pesticide treated seed through ethanol processing that produces solid and liquid byproduct waste highly contaminated with pesticide residues. Furthermore, these byproducts were distributed a     s soil conditioners to local farmers. The NE Department of Ag (NDA) and EPA estimate when “applied at 20 tons per acre, with a clothianidin concentration of 427,000 ppb, would result in 17.08 lbs. of active clothianidin applied per acre which is 85 times the maximum annual field load allowed by a typical register pesticide label.” The highest level documented in the NDA reports was 556,000 ppb clothianidin detected in distiller’s grain collected from the harvester. The report also noted the ethanol plant manager stated that the collected sample “was ready for land application”. In response to this issue, UNL formed a working group consisting of researchers, regulatory officials, stakeholders, and legal experts to help understand the regulatory, legal, and research challenges and help identify research priorities, funding opportunities, immediate action steps, and long-term goals. The working group consists of over twenty professionals, non-profit partners, legal experts, students and researchers including three NC1173 members (Wu-Smart (UNL), Spivak (UMN), Johnson (OSU). Drs. Michelle Hladik (USGS-California) and Dan Snow (UNL Water Science Lab) have been assisting with pesticide analyses of water, soil, vegetation, and hive samples collected on site. Given the complexity of both the research and policy challenges, UNL will hire someone to coordinate discussions among state agencies, researchers, external partners, and stakeholders and to specifically help us coordinate targeted research with One Health collaborators in spring 2021 (through stakeholder funding via Project Apis m./The National Honey Board funds (~$60K for one year)). Efforts will prepare the working group to gather preliminary data and identify research priorities for future USDA/EPA funding. UNL is also working with officials from NE Department of Ag, NE Department of Environment & Energy, and US EPA to report our bee loss data and better understand the regulatory process and enforcement oversight for the contaminated liquid effluent and solid byproducts generated during this ethanol process. Below is a Guardian article recently published regarding this local issue that has national implications. <a href="https://amp.theguardian.com/us-news/2021/jan/10/mead-nebraska-ethanol-plant-pollution-danger">https://amp.theguardian.com/us-news/2021/jan/10/mead-nebraska-ethanol-plant-pollution-danger</a> In addition, The Danforth lab (Cornell) conducted a series of experiments to determine how a widely-used fungicide (cyprodinil) impacts larval development in a common, easily-manipulated, mason bee (Osmia cornifrons; Megachilidae). They developed two experiments to specifically determine how fungicides impact the normal progression of larval development and whether the fungicidal treatments impacted the microbial community of the pollen provisions upon which these larvae are feeding. In addition, the TAMU bee lab (Rangel, Texas A&M University) wrapped up a project looking at the effects of pesticide exposure on honey bee queen and drone reproductive health. They looked at whether exposure of queen and drone larvae to wax contaminated with field relevant concentrations of miticides and agro-chemicals affected sperm count and viability, size, queen egg-laying capacity, chemical composition of queen mandibular gland pheromones, and ovariole size. Short outcomes, Objective 1b: The PSU team, (1) identified plant species that are preferred by honey bees for foraging in urban areas, (2) demonstrated that ornamental plant species can serve as important forage resources for managed and wild bees, but there is considerable variation among cultivars (Grozinger, Patch). (3) demonstrated that landscape toxic load has increased dramatically over the past 20 years, particularly in regions of the US that are dominated by field crops that use neonicotinoid seed treatments, and (4) provided an analysis-ready, 14 year data set of wild bee populations in mid-Atlantic (Grozinger). Likewise, the research team including Rangel (TAMU), Huang (MI State) and Ellis (UF) analyzed the pesticides present in nectar and pollen samples in urban and suburban areas across the U.S. Williams (Auburn, AL) and team observed that drones are possibly more susceptible to abiotic stressors like neonicotinoids compared to unexposed drones. This may be explained by the haploid susceptibility hypothesis. Lastly The insights gleaned from the studies carried out at Oregon State University on honey bee nutrition have advanced the understanding of sterol metabolism and regulation in honey bees and will assist in formulation of a more complete artificial diet for honey bees (Sagili). Outputs, Objective 1b: NC1173 members (Grozinger & Patch -PSU) developed an insecticide toxic load index, which integrates data from multiple government databases to provide a measure of the total toxicity of all the pesticides applied to a particular crop in a particular state (Douglas et al 2020). Development of this index allowed to examine patterns in insecticide use and toxicity over the last ~20 years, and demonstrated a significant increase in toxic load, due primarily to neonicotinoid seed treatments. This index has been incorporated into our Beescape portal (see Obj3 below) and is being used in large scale analyses of bee health. Objective 2: (Genetics, Breeding, & Diversity) Breeding mite and disease resistant traits in honey bee stock and diversifying honey bee genetics and selection efforts are more sustainable solutions to address the pest and pathogen issues in honey bees and is a long-term goal for NC1173 members. Efforts include studies to examine how establishing high-yield nectar crops support high densities of honey bee colonies required for mating yards in honey bee genetic improvement programs (Eitzer, Stoner, Cowles -Connecticut Ag Station; Harpur Purdue University) and breeding and selection of high grooming/mite biting behavior in Ohio feral colonies (Li-Byarlay, CSU). Sheppard and the WSU team continued selection and maintenance of  the New World Carniolan strain of honey bee, including inputs of cryopreserved A. m. carnica germplasm from Slovenia origin.  They produced and supplied instrumentally inseminated (i. i.) “breeder” queens to a number of commercial queen producers of open-mated NWC “production” queens. Together with industry partners, WSU initiated a plan to hand off the production of i. i. New World Carniolan i. i. breeder queens to commercial queen producers in 2021. Starting in 2021, NWC breeder queens supplied to the queen production industry will come from queen producer partners (rather than WSU) and WSU will be responsible for maintenance of the genetic stocks and infusion of A. m. carnica genetics from our repository of cryopreserved Old-World semen. In addition, WSU continued selection and distribution of a Caucasian strain of honey bees derived from Old-World origins. Using cryopreserved semen from collections of A. m. caucasica germplasm made over the past decade in the country of Georgia. WSU continues its effort to reintroduce this strain of honey bee to US beekeepers. In 2020 we supplied i.i. breeder queens to a number of commercial queen producers, who produced open-mated daughters for sale throughout the US. This strain is especially interesting to beekeepers from colder climates within the US (Sheppard, WSU). Keith Delaplane’s group (U Georgia) along with Debbie Delaney’s (U Delaware) completed a 2-year NIFA CPPM-funded project examining interactions of VSH-selected drone semen with polyandry (queens inseminated with 9 or 54 males). Colony mite levels increased in wild-type lines as one moved from polyandry=9 to =54, but decreased in VSH lines from polyandry=9 to =54, consistent with published theory that hyperpolyandry evolves under the influence of rare, beneficial alleles. Colony survival rates were highest in queens/colonies inseminated with VSH semen at the 54-drone polyandry rate. Additionally, polyandry, irrespective of semen source, significantly increased colony bee populations and comb construction rates. These results support the practice of more intentionally integrating high mating numbers with targeted trait selection efforts. Delaplane and Delaney also partnered with Geoff Williams (Auburn) in a FFAR-funded project to examine the use of inter-colony brood mixing as a beekeeper-friendly proxy method for obtaining colony benefits of hyperpolyandry. Short outcomes, Objective 2: Purdue University (Hapur) breeding program with mite resistant traits has been successfully made available in seven US States. Harpur has secured funding (Eva Crane Trust) to explore the genetic diversity of honey bees across the United States to understand baseline levels of genetic diversity. In addition, Harpur and Lopez-Uribe secured a USDA AFRI (USDA AFRI 102265) to determine how different honey bee genetic lines perform in the hands of beekeepers.  Selection and breeding for high grooming and mite biting behavior from Ohio feral colonies, evaluation queen development (48-hr queen cells) and egg laying rate of different honeybee stocks, work with 30 Ohio beekeepers to collect different wild colonies, and collaborate with Purdue University on mite biters as satellite breeding site via instrumental insemination (Li-Byarlay CSU). NC1173 members (Ellis, UF) are working with collaborators to develop a stock certification program for honey bees in Puerto Rico. Harpur (Purdue) and Lopez-Uribe (PSU) received a USDA-CARE grant to compare the performance of different honey bee stocks in different regions of the MidAtlantic. The project involves the participation of 30 beekeepers in IN and PA. PSU NC1173 members Grozinger and Rasgon are developing tools for genetic manipulation/transformation of bees (State), which will facilitate the identification and validation of genetic markers for bee health and behavior; this project is funded by the NSF-EDGE program. Grozinger (PSU) worked with Nino (UCD) on a project that demonstrated that seminal fluids can trigger post-mating changes in honey bees queens when injected into the abdominal cavity, suggesting these target receptors are outside of the reproductive tract, as is the case in Drosophila (Grozinger, PSU, and Nino, UCD). NC1173 members at NC State have investigated how different honey bee stocks (genotypes) can respond differentially to a suite of pesticide exposure (Rinkevich, Tarpy, NCSU). These findings highlight the need to control for not just environmental context but genetic background as well when conducting toxicological and physiological assessments of honey bees. Outputs, Objective 2: NC1173 members worked directly with over numerous beekeepers and nearly through  extension programs and courses, which were mostly virtual in 2020. CSU provided extension talks to 620 beekeepers and general public including four extension webinars at CSU, plenary talk at two regional agricultural and beekeeping conference, one scientific publication on mite biting behavior and mite-resistance in review (Li-Byarlay, CSU). Sagili and team at OSU organized a virtual conference for Western beekeepers. Flenniken and other NC1173 Members gave presentations to the Bee Inform     ed Tech Transfer team. Objective 3: (Management) Management practices to maintain healthy honey bees and landscapes that support pollinators are in high demand and recommendations continue to evolve with new research. Therefore, NC1173 members strive to engage with stakeholders to better provide the most up-to-date, science-based recommendations to beekeepers, pesticide applicators, farmers, homeowners and policy makers. Recommendations include how to better manage pests and pathogens in honey bees, enhancing landscapes for pollinators, and options to reduce exposure or mitigate effects of pesticides. NC1173 members conducted studies to identify the most attractive and nutritionally beneficial species of plants in urban (Sponser et al 2020, Erickson et al 2020) and agricultural or semi-natural settings (Treanore et al 2019, Russo et al 2020). NC1173 members (McLaughlin, Hoover and Grozinger PSU) conducted studies in Spring 2020 to define the pollinator communities for black cherry, a key timber species in northeastern forests suffering from declining regeneration, and the environmental factors that influence pollinator abundance and diversity. Using a combination of passive and active sampling techniques, pollinators were collected from flowering black cherry trees in the Allegheny National Forest and in State College, PA. PSU team members analyzed pollen macronutrients from 82 plant species and collected pollen from three bee species to demonstrate that there is considerable variation in the protein:lipid ratios, thus potentially allowing us to select plants that provide optimal nutrition for different bee species (Grozinger, Patch, Hines). Short outcomes, Objective 3: NC1173 members (López-Uribe and Underwood PSU) have worked with a group of 30 beekeepers to develop the protocol for best management practices for beekeepers that have different philosophies towards chemical treatments (Underwood et al 2019). NC1173 members (McLaughlin, Hoover and Grozinger PSU), found that key pollinators of black cherry, which flower in May and early June depending on location, appear to be early spring bees from the family Andrenidae, but the overall pollinator community also included bees from the families Megachilidae and Halictidae, flies, and beetles. Fruit was also collected from each tree as it dropped in the early and late fall onto the forest floor surrounding our experimental trees, and ripened fruit was tested for seed viability. Analyses are in progress to determine which variables are predictive of pollinator community morphotypes and viable seed production, which include several biotic and abiotic factors such as the presence of key pollinator communities observed directly interacting with black cherry flowers and metrics of tree health. Through collaborations, the NC State team has developed better understanding of how queen shipment, handling, and introductions are influenced by externals factors, especially temperature, and the development of predictive physiological signals that may be indicative of queen failure, which is a primary concern in apiculture management (Pettis, Tarpy, NC State). They also started a new collaborative paradigm on the variation in egg size as a function of hive size and other management factors (Rueppell, Tarpy, NC State). Williams (Auburn, AL) performed a citizen science experiment, and documented the negative effects of the COVID-19 pandemic on bee research and extension activities. As expected, there were significant disruptions in spring 2020, including travel associated with scientific communication and networking, as well as field work. Sagili (OSU) synthesized a Survey-derived best beekeeping management practices to improve colony health and reduce mortality. These studies related to honey bee colony management provide additional tools/practical methods for beekeepers to enhance colony health and survival. Outputs, Objective 3: Wild Honey Bees in Community Environments – Identification, Biology, and Reducing Risks Shaku Nair, Dawn H. Gouge, Ayman Mostafa ,Shujuan Li, Kai Umeda, Hongmei Li-Byarlay, 2020, <a href="https://extension.arizona.edu/pubs/wild-honey-bees-community-environments-%E2%80%93-identification-biology-reducing-risks">https://extension.arizona.edu/pubs/wild-honey-bees-community-environments-%E2%80%93-identification-biology-reducing-risks</a> Penn State Extension offered weekly two webinars series in 2020. During the 75-minute live webinars, there is an interactive Q&A session. The webinars reached over 8,000 participants from all states in the United States, and 16 countries around the world. Topics for the webinars included several aspects of bee diversity, bee management, and stressors related to bee decline.Lopez-Uribe and Underwood have developed a highly effective protocol for managing honey bee colonies using organic approaches. The details of this approach has already been disseminated through webinars, talks to beekeeping clubs, and there is an upcoming extension publication with the details of this protocol.  PA Pollinator Protection Plan (led by Boyle, includes all faculty members.  We worked together with a team of 36 individuals representing 28 state- and national-organizations and stakeholder groups to develop the Pennsylvania Pollinator Protection Plan (P4). Dr. Natalie Boyle organizes meetings of the P4 group every 4 months. Beescape (Grozinger). In April 2019, we launched an online tool called “Beescape” (beescape.org), which allows users (across the continental US) to explore landscape quality (forage quality, nesting habitat quality for wild bees,  for bees at their selected sites. Using  wintering colony survival data from the Pennsylvania State Beekeepers Association Survey (Calovi et al, 2021). we developed a new decision support tool, BeeWinterWise. K-12 students. With Penn State’s Center for Science and the Schools, we received funding from the USDA-PD-STEP program to develop programming targeting k-12 teachers from underserved rural and urban communities. We created lesson plans and other content that are available online (Grozinger, Patch, Boyle; Penn State’s Center for Pollinator Research). With faculty in Penn State’s Learning, Design and Technology Program we developed a 1 hour workshop for families with pre-K through middle school children for use in rural libraries and museums (Grozinger). We have conducted several school visits, and presentations as part of the PSU “Nature Explorers” summer camp (elementary school) and the Pennsylvania School of Excellence in Agricultural Sciences high school summer program (Hines).Patch (PSU) is leading the development of a >4 acre Pollinators and Bird Garden at the Arboretum at PSU, which will feature 400 plant types and serve as a venue to showcase research on plant-pollinator interactions and conservation.  The garden will open in spring 2021 and is expected to welcome 100K visitors each year. Impacts Oregon State University (Sagili). The Oregon Master Beekeeper Program serves the needs of both backyard and commercial beekeepers in Oregon and Idaho. This is the first program in the USA with unique hands on training (mentor-mentee type). This program has received an overwhelming response since its inception in 2011. Currently there are more than 1,700 registered participants and a long wait list. The program has educated and trained commercial beekeepers in the state that pollinate about 90% of the crops, as well as extension agents, beginner beekeepers, farmers, Oregon Department of Agriculture and USDA field personnel (NRCS). Four other states in the USA have sought our assistance for starting their new MB programs based on our model. Oregon Master Beekeeper Program was cited a unique Master Beekeeper Program in the country (Western Apicultural Society Journal, August 2019, American Bee Journal 2020). University of Nebraska-Lincoln (Wu-Smart). In 2020, UNL Bee Lab provided 6 beekeeping workshops across four major Nebraska cities. These workshops included 5 introductory level classes (Year 1 & Year 2 Beekeeping) to 673 new or aspiring beekeepers to educate about basic honey bee management and IPM strategies for honey bee pests/diseases. Some Jan-Mar courses were offered in-person, but all others were quickly converted to virtual programs for Covid-19 safety. Current membership in the Great Plains Master Beekeepers (GPMB)Training Program (website: <a href="https://gpmb.unl.edu/">https://gpmb.unl.edu/</a>) is now 840 participants and 51% are women (Demographics: 409 Male, 429 Female, 689 Caucasian, 17 African American, 9 Tribal members, 46 Latinx, 22 Other, 156 Military. Through GPMB, we have recruited new partnering beekeeping groups and certified the first 9 “master” and 2 “journeymen” level beekeepers. Certified Masters may now proctor field exams in their own representative states for GPMB (Project Funded through USDA BRFD # 2018-70017-28546). In 2020, UNL Bee Lab and GPMB course participants included beekeepers across 8 states (NE, KS, IA, CO, SD, WY, and MO). From pre- and post-course evaluations, 98.5% of participants (390/396) responded they would recommend our beekeeping courses. Furthermore, 65.6% of participants responded they intend to expand their business because of our value-added course offerings. At the beginning of 2020, about 67% responded they treat for mites and at the end of the year we saw an increase (70% of respondents) in participants who now implement integrated pest management approaches for mites. When asked “What changes in your beekeeping operation will you enact after this class?” several responded they intend to implement these practices.  (Example responses: “I will take all the information presented within this module to my own experiences. One thing that stood out to me that I plan on doing is making sure to treat hives for mites even if we do not visibly see them. (Year1)”;“I will have a better assessment on how to inspect hives which would allow me to better help and increase the hive's condition.(Year2)”; “Definitely add the Dead Bee Traps! Will definitely start using your Inspection sheets. Also, I'm glad to hear that you support the sugar roll method (Varroa IPM short course)”; “Love the hands on training so far.  Speakers always make the students feel comfortable enough to ask any question no matter the level of beekeeper (Year 2).” In 2021, UNL will continue to expand extension training      and focus on program sustainability. UNL has already started working with external partners from Michigan State University to establish a targeted program for military veterans (“Heros to Hives”) in Nebraska and are seeking continuation funding for GPMB efforts. 2020 Virtual Programs: In response to cancelled in-person training UNL developed, organized, and delivered several virtual learning alternatives. The most notable have been included below: (1) GPMB Virtual Fun Day: In 2020, all partnering beekeeping associations had to cancel their annual summer bee fun day events so GPMB responded by delivering a Virtual Bee Fun Day webinar to give our partner organizations and GPMB members an educational outlet during the Covid-19 quarantine. Over two days (June 13-14, 2020) we provided ~16 hours of lectures, field demonstrations, and maker’s workshop classes. We had 681 registered participants, and 23 speakers from research & academic institutions (n=7), extension professionals (n=5), non-profit organizations (n=1), graduate students (n=2), and local professional beekeepers (n=8). Of the 23 speakers, 10 are NC1173 members and or active AAPA members. With no less than 190 attending at any given time throughout the day, the turnout was quite large, and feedback was very positive regarding the breadth of topics covered from basic hive management to how honey bee artificial insemination works. (<a href="https://unl.box.com/s/vm6u281xm6rpfoney1lbb75qdw4a2z5e">See Program Schedule</a>). Due to Covid-19, we did not charge for this program, but suggested participants may contribute $10 donations/per person to sustain future GPMB efforts. We received 105 gifts ranging from $2-$200 and raised a total of $3,233 ($3,103.68 after 4% fees). Participants were given the option to also donate to their local beekeeping associations, so partners received some revenue as well. For more information: <a href="https://gpmb.unl.edu/">https://gpmb.unl.edu/</a> (2) Virtual Hap-Bee Hour Chats: We collaborated with Randall Cass from Iowa State University Extension to offer weekly virtual open discussions. Hap-Bee Hour was offered weekly from April through November (30+ sessions; every Friday 5-6 pm via Zoom) and now offered monthly. The informal virtual gathering allowed beekeepers to share photos, videos, and discuss problems and we prepared seasonal tips to help beekeepers keep up with hive management needs. There were ~20-40 participants from NE, IA, KS, MO and CA and recordings of the Hap-Bee Hour chats are archived and made available online. (3) Girls Scouts of NE “The Good, the Bad, and the Ugly”: This 3-day program (targeting 4-12th graders) was developed in collaboration with the Girls Scouts, Kimmel Orchard, UNL Entomology (J. Wu-Smart & L. Lynch O’Brien), NE State Arboretum, and the NE Depart. of Agriculture was delivered in July and August 2020. Each participant received teaching kits with live pollinator plants, bee nest materials, aquatic insect and invasive insect monitoring tools and resources to complement virtual lessons (<a href="https://unl.box.com/s/467ie4bzkeawlxho95bbr5kq19ya32z3">Program link</a>). We reached 55 students from across 18 states (34% from Nebraska; (18% from west coast CA, OR), (18% from east coast MD, NC, RI, VA), and (5.5% from south FL, TX)) as well as representation from 9 additional states (23.6% from CT, GA, IL, MO, NJ, NY, OH, PA, SC) (Partially funded through the US EPA Environmental Education Grant #123268). Central State University (Li-Byarlay) received USDA-SARE grant from North Central Region to investigate the possibility of using 48-hr queen cells to help beekeepers to diversify honeybee genetics in their own apiaries and increase their colonies collections with mite-resistance trait such as high grooming and mite biting. Working with extension, CSU bee lab provided four online webinars on sustainable beekeeping by using swarm traps, queen development, decreasing viral infections and temperature control.

Publications

Summary table and list of publications by topic reported by NC1173 committee members for 2020. NC1173 authors are indicated in bold. <table width="557"> <tbody> <tr> <td width="461"> Publications by topic </td> <td width="96"> 2020 </td> </tr> <tr> <td width="461"> Obj 1a: Biotic (Pests & pathogens) </td> <td width="96"> 21 </td> </tr> <tr> <td width="461"> Obj 1b: Abiotic (Pesticides, nutrition, landscapes) </td> <td width="96"> 31 </td> </tr> <tr> <td width="461"> Obj 2: Genetics, Breeding, Diversity </td> <td width="96"> 9 </td> </tr> <tr> <td width="461"> Obj 3: Management </td> <td width="96"> 10 </td> </tr> <tr> <td width="461"> Other Publications </td> <td width="96"> 4 </td> </tr> <tr> <td width="461"> Total </td> <td width="96"> 75 </td> </tr> <tr> <td width="461"> Publications with >1 NC1173 authors </td> <td width="96"> 17 </td> </tr> </tbody> </table> NC1173 Member Publications (01/01/2020 to 12/31/2020) *Papers applicable to multiple objectives are only reported once Metz BN, Wu-Smart J, Simone-Finstrom M. 2020. Proceedings of the 2020 American Bee Research Conference. Insects 11(6):362. Simone-Finstrom, M., Nino, E., Flenniken, M., Wu-Smart, J. 2020. Proceedings of the 2019 American Bee Research Conference. Insects 11(2):88. Objective 1a: Biotic Stressors (Pests & pathogens) Faurot-Daniels#, C., I., Glenny#, W., Daughenbaugh, K.F., McMenamin, A.J., Burkle, L., and Flenniken, M.L., Longitudinal monitoring of honey bee colonies reveals dynamic nature of virus abundance and indicates a negative impact of Lake Sinai virus 2 on colony health, (2020), #equal co-authorship, PLoS ONE, doi: 10.1371/journal.pone.0237544. eCollection 2020 McMenamin, A.J., Daughenbaugh, and Flenniken, M.L, The Heat Shock Response in the Western Honey Bee (Apis mellifera) is Antiviral, (2020), Viruses, 12, 245; doi:10.3390/v12020245. Amiri, E., J. J. Herman, M. K. Strand, D. R. Tarpy, and O. Rueppell. (2020). Egg transcriptome profile responds to maternal virus infection in honey bees, Apis mellifera. Infection, Genetics and Evolution, 85: 104558. Li-Byarlay, H., H. Boncristiani, G. Howell, M. K. Strand, D. R. Tarpy, and O. Rueppell. (2020). Transcriptome and epigenome dynamics of honey bees in response to lethal virus infection. Frontiers in Genetics, 11: 566320. Kevill, J.L., K. Lee, M. Goblirsch, E. McDermott, D. R. Tarpy, M. Spivak, and D. C. Schroeder. (2020). The pathogen profiles of queen honey bees does not reflect those of their colonies workers. Insects, 11: 382. Amiri, E., C., M. K. Strand, D. R. Tarpy, and O. Rueppell. (2020). Honey bee queens and virus infections. Viruses, 12: 232. doi:10.3390/v12030322. López-Uribe MM, Ricigliano V, Simone-Finstrom MD (2020) Defining Pollinator Health: Understanding bee ecological, genetic and physiological factors at the individual, colony and population levels. Annual Review of Animal Bioscience. doi:10.1146/annurev-animal-020518-115045 McNeil, D.J., E. McCormick, A. Heimann, M. Kammerer, M. Douglas, S.C. Goslee, C.M. Grozinger, and <ol start="2020"> <li> M. Hines. 2020. Bumble bees in landscapes with abundant floral resources have lower pathogen loads. Nature Scientific Reports.</li> </ol> Ray, A.M., Lopez, D.L., Martinez, J.F., Galbraith, D.A., Rose, R., vanEngelsdorp, D., Rosa, C., Evans, J.D., and C.M. Grozinger. (2020) “Distribution of recently identified bee-infecting viruses in managed honey bee (Apis mellifera) populations in the United States” Apidologie DOI: 10.1007/s13592-020-00757-2. Liu, F.*, X. Xu, Y. Zhang, Z.Y. Huang *, H. Zhao. 2020. A meta-analysis shows that screen bottom boards can significantly reduce Varroa destructor population. Insects, 11(9): 624. doi: <a href="https://dx.doi.org/10.3390%2Finsects11090624">10.3390/insects11090624</a>. Chapter Two - Current trends in the oxidative stress and ageing of social hymenopterans H Li-Byarlay, XL Cleare, Advances in Insect Physiology 59, 43-69, 2020. Jennifer O. Han, Nicholas L. Naeger, Brandon K. Hopkins, David Sumerlin, Paul E. Stamets, Lori M. Carris, and Walter S. Sheppard. .  Directed evolution of Metarhizium fungus improves its biocontrol efficacy against Varroa mites in honey bee colonies. Submitted to Current Biology Brandon K. Hopkins, Jason Long, and Walter S. Sheppard.  Comparison of indoor (refrigerated) vs outdoor winter storage of commercial honey bee (Apis mellifera) colonies in the Western US. Submitted to J. Econ. Entomol. Jack, C.J., van Santen, E., Ellis, J.D. 2020. Evaluating the efficacy of oxalic acid vaporization and brood interruption in controlling the honey bee pest Varroa destructor (Acari: Varroidae). Journal of Economic Entomology, 113(2): 582-588. <a href="https://doi.org/10.1093/jee/toz358">https://doi.org/10.1093/jee/toz358</a>. Papach, A., Williams, G.R., Neumann, P., 2020. Evolution of starvation resistance in an invasive insect species, Aethina tumida (Coleoptera: Nitidulidae). Ecology and Evolution 10, 9003-9010. Huwiler, M., Papach, A., Cristina, E., Yañez, O., Williams, G.R., Neumann, P., 2020. Deformed wings of small hive beetle independent of virus infections and mites. Journal of Invertebrate Pathology 172, 107365. Bird, G., Wilson, A.E., Williams, G.R., Hardy, N.B., 2020. Parasites and pesticides act antagonistically on honey bee health. Journal of Applied Ecology https://doi.org/10.1111/1365-2664.13811. Accepted 7 December 2020. Spivak M, Danka RG. 2020. Perspectives on hygienic behavior in Apis mellifera and other social insects.  Apidologie DOI: 10.1007/s13592-020-00784-z 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 Spivak M, Cariveau DP. 2020. Flowers as parasite transmission hubs. Nat Ecol Evol. <a href="https://doi.org/10.1038/s41559-020-1200-z">https://doi.org/10.1038/s41559-020-1200-z</a> 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 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 Iwanowicz DD, Wu-Smart, JY, Olgun T, Smart, AH, Otto, CR, Lopez, D, Evans, JE, Cornman R. 2020. An updated genetic marker for detection of Lake Sinai Virus and metagenetic applications. Peerj   8:e9424. DOI: 10.7717/peerj.9424. Olgun T, Everhart SE, Anderson T, Wu-Smart J. 2020. Comparative analysis of viruses in four bee species collected from agricultural, urban, and natural landscapes. PLoS ONE 15(6): e0234431.   Objective 1b: Abiotic Stressors (Pesticides, nutrition, landscapes) Vaudo AD, Biddinger DJ, Sickel W, Keller A, López-Uribe MM. (2020) Phylogenetic pollen preferences facilitate naturalization and pollination services of introduced bees in new habitats. Royal Society Open Science 7(7):200225 doi/10.1098/rsos.200225 Phan N, Joshi N, Rajotte E, López-Uribe MM, Zhu F, Biddinger DJ. (2020) A new ingestion bioassay protocol for assessing pesticide toxicity to the adult Japanese orchard bee (Osmia cornifrons) Scientific Reports. <a href="https://doi.org/10.1038/s41598-020-66118-2">https://doi.org/10.1038/s41598-020-66118-2</a> Villalona, E., B.D. Ezray, E. Laveaga, A.A. Agrawal, J.G. Ali, and H.M. Hines. 2020. The role of toxic nectar secondary compounds in driving differential bumble bee preferences for milkweed flowers. Oecologia. Vaudo, A. D., J. F. Tooker, H. M. Patch, D. J. Biddinger, M. Coccia, M. K. Crone, M. Fiely, J. S. Francis M. Hines, M. Hodges, S. W. Jackson, D. Michez, J. Mu, L. Russo, M. Safari, E. D. Treanore, M. Vanderplanck, E. Yip, A. S. Leonard, and C. M. Grozinger. 2020. Pollen protein:lipid macronutrient ratiosguide broad patterns of bee species floral preferences. Insects, (11):132. Feliciano-Cardona, S., Döke, M.A., Aleman-Rios, J., Agosto-Rivera, J.L., Grozinger C.M., and T. Giray. 2020.  “Honey bees in the tropics show winter bee-like longevity in response to seasonal dearth and brood reduction” Frontiers in Ecology and Evolution 8:336 Sponsler, D.B., Shump, D., Richardson, R., Grozinger, C.M. (2020) “Characterizing the floral resources of a North American metropolis using a honey bee foraging assay”  Ecosphere 11(4): e03102 DOI: <a href="https://doi.org/10.1002/ecs2.3102">10.1002/ecs2.3102</a> (2020). Sponsler, D.B., Grozinger, C.M., Richardson, R., Nurse, A., Brough, D., Patch, H.M., and K. A. Stoner. (2020) " A screening-level assessment of the pollinator-attractiveness of ornamental nursery stock using a honey bee foraging assay" Scientific Reports 10(1), 1-9. Russo, L., Keller, J., Vaudo, A., Grozinger, C.M., K. Shea. (2020) “Warming increases pollen lipid concentration in an invasive thistle, with minor effects on the associated floral-visitor community”  Insects 11(1) 20. Erickson, E., Adam. S., Russo, L., Wojcik, V., Patch, H.M., and C.M. Grozinger. (2020) “More than meets the eye: The role of ornamental plants in supporting pollinators” Environmental Entomology 49(1) 178-188. POL-10-W - Harpur, B. A. 2020. Indiana Solar Site Pollinator Habitat Planning Scorecard. Danforth, B.N., R.L. Minckley, J.L. Neff (2019). The Solitary Bees: Biology, Evolution, Conservation. Princeton, NJ: Princeton University Press Saleem, M.S.,  Z.Y. Huang*, M. Milbrath. 2020. Neonicotinoid pesticides are more toxic to honey bees at lower temperatures: implications for overwintering bees. Frontiers in Ecology and Evolution, <a href="https://doi.org/10.3389/fevo.2020.556856">https://doi.org/10.3389/fevo.2020.556856</a>. Krichilsky, E, M. Centrella, B. Eitzer, B.N. Danforth, K. Poveda, H. Grab (2020). Landscape composition and fungicide exposure influence host-pathogen dynamics in a solitary bee. Environmental Entomology [published online 28 Nov, 2020: https://doi.org/10.1093/ee/nvaa138] Keller, A. Q.S. McFrederick, P. Dharampal, S. Steffan, B.N. Danforth, S.D. Leonhardt (2020). (More than) Hitchhikers through the network: The shared microbiome of bees and flowers. Current Opinions in Insect Science [published online Sept. 29, 2020; DOI: https://doi.org/10.1016/j.cois.2020.09.007] Centrella, M., L. Russo, N. Moreno-Ramirez, B. Eitzer, M. Van Dyke, B.N. Danforth, K. Poveda (2020). Landscape simplification reduces solitary bee performance in agroecosystems via increased pesticide exposure, reduced floral diet diversity, and their interaction. Journal of Applied Ecology 2020;00:1–12. https://doi.org/10.1111/1365-2664.13600 [published online 23 February, 2020]. Camp AA, Williams, WC, Eitzer, BD, Lehmann DM. (2020). Effects of the Neonicotinoid Acetamiprid in Syrup on Bombus impatiens (Hymenoptera: Apidae) Microcolony Development.  PLOS One. 15(10):e0241111. doi: 10.1371/journal.pone.0241111 Camp AA, Batres MA, Williams, WC, Stoner, KA, Koethe, R, Lehmann DM. (2020). The neonicotinoid acetamiprid in pollen impacts Bombus impatiens (Hymenoptera: Apidae) microcolony development.  Environ Toxicol Chem. 39(12):2560-2569. doi: 10.1002/etc.4886. McAfee, A., A. Chapman, H. Higo, R. Underwood, J. Milone, L. Foster, M. M. Guarna, D. R. Tarpy, and J. S. Pettis. (2020). Honey bee queens are vulnerable to heat-induced loss of fertility. Nature Sustainability, 3: 367-376. CYP6AS8, a cytochrome P450, is associated with the 10-HDA biosynthesis in honey bee (Apis mellifera) workers Y Wu, Y Zheng, H Li-Byarlay, Y Shi, S Wang, H Zheng, F Hu, Apidologie 51 (6), 1202-1212, 2020 Tomé, H.V.V., Schmehl, D.R., Wedde, A.E., Godoy, R.S.M., Ravaiano, S.V., Guedes, R.N.C., Martins, G.F., Ellis, J.D. 2020. Frequently encountered pesticides can cause multiple disorders in developing worker honey bees. Environmental Pollution, 256(1): 113420. <a href="https://doi.org/10.1016/j.envpol.2019.113420">https://doi.org/10.1016/j.envpol.2019.113420</a>. Friedli, A., Williams, G.R., Bruckner, S., Neumann, P., Straub, L., 2020. The weakest link: Haploid honey bees are more susceptible to neonicotinoid insecticides. Chemosphere 242, 125145. Topitzhofer, E., Lucas, H.M., Carlson, E.A., Chakrabarti, P., Sagili, R.R. (2021) Collection and Identification of Pollen from Honey Bee Colonies. Journal of Visualized Experiments DOI: 10.3791/62064. Milone, J.P., Chakrabarti, P., Sagili, R.R. and Tarpy, D.R. (2021) Colony-level pesticide exposure affects honey bee (Apis mellifera L.) royal jelly production and nutritional composition. Chemosphere 263: 128183. Chakrabarti, P. and Sagili, R.R. (2020) Changes in Honey Bee Head Proteome in Response to Dietary 24-Methylenecholesterol. Insects 11(11): 743. Chakrabarti, P., Carlson, E.A., Lucas, H.M., Melathopoulos, A.P. and Sagili, R.R. (2020) Field rates of Sivanto™ (flupyradifurone) and Transform® (sulfoxaflor) increase oxidative stress and induce apoptosis in honey bees (Apis mellifera L.). PLoS ONE 15(5): e0233033. Chakrabarti, P., Lucas, H.M. and Sagili, R.R. (2020) Novel Insights into Dietary Phytosterol Utilization and Its Fate in Honey Bees (Apis mellifera L.). Molecules 25: 571. DOI: 10.3390/molecules25030571. Reilly JR, Artz DR, Biddinger D, Bobiwash K, Boyle NK, Brittain C, Brokaw J, Campbell JW, Daniels J, Elle E, Ellis JD, Fleischer SJ, Gibbs J, Gillespie RL, Gundersen KB, Gut L, Hoffman G, Joshi N, Lundin O, Mason K, McGrady CM, Peterson SS, Pitts-Singer TL, Rao S, Rothwell N, Rowe L, Ward KL, Williams NM, Wilson JK, Isaacs R, and Winfree R. 2020. Crop production in the USA is frequently limited by a lack of pollinators. Proceedings of the Royal Society of London B 287: 20200922.  doi.org/10.1098/rspb.2020.09222020 Reilly et al ProcB paper was featured in The Guardian (USA), Forbes, Science News 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 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 Spivak M, Mendel B. 2020. Propolis for Bees.  2millionblossoms.com Vol 1. Walsh EM*, Janowiecki MA*, Zhu K**, Ing NH, Vargo EL, Rangel J (2020) Elevated mating frequency in honey bee (Hymenoptera: Apidae) queens exposed to the miticide amitraz during development. Annals of the Entomological Society of America. DOI: 10.1093/aesa/saaa041. Walsh EM*, Sweet S, Knap A, Ing NH, Rangel J (2020) Queen honey bee (Apis mellifera) pheromone and reproductive behavior are affected by pesticide exposure during development. Behavioral Ecology and Sociobiology. 74: 33. DOI: 10.1007/s00265-020-2810-9.   Objective 2: Genetics, Breeding, Diversity Milone, J. P., F. R. Rinkevich, A. McAfee, L. J. Foster, and D. R. Tarpy. (2020). The influence of breeding stock on honey bee (Apis mellifera) larval pesticide tolerance, esterase activity, and proteome. Ecotoxicology and Environmental Safety, 206: 111213. Kilpatrick SK, Gibbs J, Mikulas MM, Spichiger S, Ostiguy N, Biddinger DJ, López-Uribe MM. (2020) An updated checklist of the bees (Hymenoptera: Apoidea: Anthophila) of Pennsylvania, United States of America. Journal of Hymenoptera Research <a href="https://doi.org/10.3897/jhr.77.49622">https://doi.org/10.3897/jhr.77.49622</a> Jasper, W.C., Brutscher, L.M., C.M. Grozinger and E.L. Nino. (2020) “Injection of seminal fluid into the hemocoel of honey bee queens (Apis mellifera) can stimulate post-mating changes”.  Scientific Reports 10, 11990. https://doi.org/10.1038/s41598-020-68437-w Kammerer, M., Tooker, J.F. and C.M. Grozinger.  (2020) “A long-term dataset on wild bee abundance in Mid-Atlantic United States”  Scientific Data 7, 240.  <a href="https://doi.org/10.1038/s41597-020-00577-0">https://doi.org/10.1038/s41597-020-00577-0</a> Harpur, B. A., Kadri, M. S., Orsi, R. O., Whitfield, C. W., Zayed, A. (2020). Defense response in Brazilian honey bees (Apis mellifera scutellata x spp.) is underpinned by complex patterns of admixture, Genome Biology and Evolution. DOI: <a href="https://doi.org/10.1093/gbe/evaa128">https://doi.org/10.1093/gbe/evaa128</a>. Stoner, K.A. (2020). Pollination is sufficient, even with low bee diversity, in pumpkin and winter squash fields. Agronomy 10: 1141. doi:10.3390/agronomy10081141 Rangel J, Shepherd TF+, Gonzalez AN+, Hillhouse A, Konganti K, Ing NH (2020) Transcriptomic analysis of the honey bee (Apis mellifera) queen spermathecae reveals genes that may be involved in sperm storage after mating. PLoS ONE 16(1): e0244648. DOI: 10.1371/journal.pone.0244648. Rangel J, Traver B, Stoner M, Hatter A, Trevelline B, Garza C, Shepherd T, Seeley TD, Wenzel J (2020) Genetic diversity of wild and managed honey bees (Apis mellifera) in southwestern Pennsylvania, and prevalence of the microsporidian gut pathogens Nosema ceranae and N. apis. Apidologie. DOI: 10.1007/s13592-020-00762-5.   Objective 3: Management Grozinger C.M. and A. Zayed. “Genomics for understanding and improving pollinator health in a world of multiple stressors” Nature Reviews Genetics 21: 277–291DOI: <a href="https://doi.org/10.1038/s41576-020-0216-1">10.1038/s41576-020-0216-1</a> (2020). McAfee, A., J. P. Milone, A. Chapman, L. J. Foster, J. S. Pettis, and D. R. Tarpy. (2020). Candidate stress biomarkers for queen failure diagnostics. BMC Genomics, 21: 571. Amiri, E., M. K. Strand, D. R. Tarpy, and O. Rueppell. (2020). Egg-size plasticity in Apis mellifera: honey bee queens alter egg size in response to both genetic and environmental factors. Journal of Evolutionary Biology, 33: 534–543. Sheppard, Walter S.   Honey Bee Pests. 2020.  In: Hollingsworth, C.S., editor. Pacific Northwest Insect Management Handbook. Corvallis, OR: Oregon State University. C8-C9. MacLeod, M, J Reilly, D Cariveau, M Genung, M Roswell, J Gibbs, and R Winfree. 2020. How much do rare and crop-pollinating bees overlap in identity and flower preferences? Journal of Applied Ecology 57: 413-423 Dall’Olio, R., Blacquiere, T., Bouga, M., Brodschneider, R., Carreck, N.L., Chantawannakul, P., Dietemann, V., Kristiansen, L.F., Gajda, A., Gregorc, A., Ozkirim, A., Pirk, C., Soroker, V., Williams, G.R., Neumann, P., 2020. COLOSS survey: global impact of COVID-19 on bee research. Journal of Apicultural Research 59, 731-734. Hopkins, B.K., Chakrabarti, P., Lucas, H.M., Sagili, R.R. and Sheppard, W.S. (2021) Impacts of different winter storage conditions on the physiology of diutinus honey bees (Apis mellifera L.). Journal of Economic Entomology toaa302: 1-6. https://doi.org/10.1093/jee/toaa302. Kelly Kulhanek, Steinhauer N, Wilkes J, Wilson M, Spivak M, Sagili RR, Tarpy DR, McDermott E, Garavito A, Rennich K, vanEngelsdorp D. Survey-derived best beekeeping management practices improve colony health and reduce mortality. PLoS ONE 16(1): e0245490. <a href="https://doi.org/10.1371/journal.pone.0245490">https://doi.org/10.1371/journal.pone.0245490</a>. Baker AM, Redmond CT, Malcolm SB, Potter DA. 2020. Suitability of native milkweed (Asclepias) species versus cultivars for supporting monarch butterflies and bees in urban gardens. PeerJ 8:e9823 <a href="http://doi.org/10.7717/peerj.9823">http://doi.org/10.7717/peerj.9823</a> Fei CJ, Williamson KM*, Woodward RT, McCarl BA, Rangel J (2020) Honey bee, almonds and colony mortality: an economic simulation of the U.S. pollination market. Land Economics. In press.   Other Publications Daniel Potter and students in his lab posted two national webinars with study guides on the GROW Plant Health Exchange website’s Pollinator Hub (formerly Plant Management Network): <a href="https://www.planthealthexchange.org/Pages/default.aspx">https://www.planthealthexchange.org/Pages/default.aspx</a>: “Woody Plants for Urban Bee Conservation” (D.A. Potter and B.M. Mach) and How to Build a Better Monarch Butterfly Garden (A.M. Baker and D.A. Potter). Payne AN, Shepherd TF, Rangel J (2020) The detection of honey bee (Apis mellifera) associated viruses in ants. Scientific Reports. 10: 2923. DOI: 10.1038/s41598-020-59712-x. Montoya JE, Arnold MA, Rangel J, Stein LR, Palma MA (2020) Pollinator-attracting companion plantings increase crop yield of cucumbers and habanero peppers. HortScience. DOI: 10.21273/HORTSCI14468-19.

Impact Statements

Date of Annual Report: 02/23/2022

Report Information

Annual Meeting Dates: 01/14/2022 - 01/14/2022
Period the Report Covers: 01/01/2021 - 12/31/2021

Participants

Participants Attachment:

NC1173 Annual Report 2022_final.pdf

Brief Summary of Minutes

Brief Summary of Annual NC1173 Multi-State Project Meeting

Minutes taken by Michelle Flenniken (Montana State University) and Margarita Lopez-Uribe (Penn State)

The NC1173 business meeting was conducted as part of the 2022 American Bee Research Conference (ABRC) with the American Association of Professional Apiculturists (AAPA) meeting via Zoom due to the SARS-CoV-2 pandemic. The ABRC was held for two days (Jan 13-14, 2022) and serves as the scientific program for the NC1173 multi-state group.

An agenda for the ABRC meeting is online (https://aapa.cyberbee.net/abrc-2021/), was submitted in conjunction with this report, and proceedings will be published in the coming months.

The business meeting was called to order at 10:00 AM EST by chairperson Dr. Michelle Flenniken from Montana State University. Attendance was recorded via zoom login information. Dr. Michelle Flenniken reviewed the current status of the multi-state project. The new Project Director / Administrative Advisor, Dr. Brian McCornack (Kansas State University), was introduced to the group and he briefly introduced himself to our team. Michelle reported that there are currently 40 members listed in NIMMS (14 of whom were in attendance) representing 27 institutions. In addition, Tom Welsh, Margaret Couvillon, Jennifer Tsuruda, Autumn Smart, and Esmaeil Amiri, who is a new Asst. Prof. at Mississippi State University joined the meeting too. Dr. Michelle Flenniken reminded members to submit their publications, activities, and milestones, so that these efforts may be reported in the 2021 NC1173 report due within 60 days of the meeting. She also encouraged members to give specific impactful one-or-two-line examples of NC1173 successes for USDA Program Directors. Dr. Judy Wu-Smart reminded the group highlight joint multi-state and/or multi-institution achievements.

Dr. Michelle Flenniken reported that the previous NC1173 report was submitted in February 2021. Next year Dr. Brian McCornack will highlight components from the 2020 and 2021 reports at the NC1173 business meeting. Dr. Christina Hamilton, the other NC1173 Administrative Advisor did not join us this year.

Dr. Erica Kistner-Thomas provided an update on USDA-NIFA-AFRI opportunities. She reported that since their move to Kansas City, Missouri, they have hired many new people after a dramatic loss in staff (i.e., ~ 80%). Dr. Kistner-Thomas was a new program leader last year, and this year other additional Entomology staff include Dr. Vijay Nandula, Lead NPL for Crop Protection and Pest Management, and Mr. Logan Appenfeller a newly hired Program Specialist. In 2021 there were 60 applications submitted to the Pollinator Health Program and funded 10 projects, including one from Dr. Lopez-Uribe was funded. The FY2021 budget included $1.95 billion dollars to NIFA, a $10 million increase in AFRI and $3 million increase to SARE. The majority of pollinator research funding has been allocated to honey bee research. This year, she saw some more bumble bee grants coming in as well. The 2022 budget has not yet been approved, but she expects it to be similar to this year and therefore a similar number of projects will be funded. Priority areas for current administration include studies that incorporate climate change and its impact on pollinators and agriculture and studies that advance racial justice, equity, and opportunity. NIFA’s pollinator research priorities include: pest and pathogen management (including Varroa IPM), bee nutrition, bee genetics and breeding, abiotic stressors including climate change and pesticides, and the role of the microbiome on bee health. Funds are also available to support pollinator extension, education, and conferences. There is funding for approximately two conference grants per year ($50,000 max each).

Dr. Erica Kistner-Thomas encouraged new faculty members who have not yet received a USDA-funded research grant and with less than 5-years of experience to apply for the “new-investigator” opportunity, with a funding level of $300,000 for up to 2-years. She also encouraged new/young investigators, including postdocs, (as well as others) to volunteer to serve on grant review panels (https://prs.nifa.usda.gov/prs/volunteerPrep.do). She noted that the maximum requires for standard USDA grants is $750,000 and the deadline for submission is August 25 at 5 pm EST (see: https://nifa.usda.gov/sites/default/files/rfa/FY-2021-2022-AFRI-Foundational-and-Applied-Science-RFA-Final-07172020.pdf). Members can contact her directly with questions (i.e., Dr. Erica Kistner-Thomas, National Program Leader, National Institute of Food and Agriculture, Institute of Food Production and Sustainability, Email: erica.kistnerthomas@usda.gov). A Question-and-Answer session followed Dr. Kistner-Thomas’s presentation and highlights from that informative session included the following: (a) a committee of stakeholders from SCRI decides what is funded via that program (see USDA-NAREE for a list of members), although you can submit two projects (e.g., a seed grant and full grant as PI) it is not encouraged (consider being a PI on one grant and a Co-PI on another).

Dr. Flenniken reiterated a decision that the next NC1173 meeting will be held with the American Bee Research Conference, which is the scientific component of the NC1173 meeting, in conjunction with the American Bee Federation (ABF) (https://www.abfnet.org/) in Jacksonville, Florida, as well as have a virtual/online option to encourage participation. In addition, Dr. Flenniken noted that she and Dr. Lopez-Uribe will strive to send out notices for ABRC and NC1173 to entire membership prior to the ABRC deadline, as well as send out virtual meeting links to entire NC1173 membership (i.e., including those that do not register / attend ABRC), this was inadvertently not done this year. Future meetings will strive to provide opportunities to interact with the American Honey Producers Association (AHPA), Canadian Association of Professional Apiculturists (CAPA), Apiary Inspectors of America (AIA) and each other. It was also noted that we should discuss ways to try to have more interaction with native/wild bee experts that do not always attend ABRC. We encourage all NC1173 members to attend ABRC, particularly when a virtual option is available. Increased notice regarding the meeting will help facilitate that. Information on future meetings is provided on the AAPA website (https://aapa.cyberbee.net/).

The floor was opened for discussion of other business. Through consensus it was decided that Dr. Michelle Flenniken will serve as NC1173 chair for two more years (i.e., through the February 2023 reporting deadline) and she will lead and be responsible for submitting the 2021 and 2022 NC1173 annual reports. For the 2022 report (in January 2023) she will get more assistance from Dr. Margarita Lopez-Uribe. Dr. Priyadarshini Chakrabarti Basu is joining the team now as the Vice-Vice Chair, so that we can better transfer duties over a longer time period and to facilitate organization and progress for renewing our NC1173 funding approval. The current funding ends in 2024, therefore this team with assistance from Dr. Judy Wu-Smart, will need to submit a renewal in 2023. Dr. Judy Wu-Smart led the efforts for our current NC1173 funding and therefore she has experience to share and she encouraged streamlining objectives to make facilitate easier and accurate reporting (i.e., since several topics intersect). The NC1173 renewal team will include: Dr. Margarita Lopez Uribe (who will be Chair in 2023), Dr. Priyadarshini Chakrabarti Basu (who will be Vice-Chair in 2023) with assistance from Dr. Michelle Flenniken (outgoing Chair in 2023) and Dr. Judy Wu-Smart (previous Chair). We will meet as a subcommittee to outline this process early with the goal of managing this effort in conjunction with our other roles. The floor was opened for discussion of other business, but in the absence of additional discussion Dr. Flenniken adjourned the meeting at 10:57 am (EST).

Minutes Attachment:

NC1173 Annual Report 2022_final.pdf

Accomplishments

NC1173 Objectives 1. To evaluate the role, causative mechanisms, and interaction effects of biotic stressors (i.e., parasitic mites, pests, and pathogens) and abiotic stressors (i.e., exposure to pesticides, poor habitat and nutrition, management practices) on the survival, health and productivity of honey bee colonies as well as within pollinator communities. 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 pathogens. 3. To develop and recommend "best management practices" for beekeepers, growers, land managers and homeowners to promote health of honey bees and pollinator communities. NC1173 Accomplishments:  Objective 1a: (Biotic Stressors: Pests & Pathogens) The Varroa destructor mite is one of the deadliest honey bee pathogens currently facing the US beekeeping industry. Varroa destructor is an ectoparasitic mite that feeds on honey bees and decimates colony populations resulting in colony death. Varroa mites also transmit viruses within and between colonies. High mite infestation coupled with high levels of viruses, including deformed wing virus (DWV), are often associated with overwinter losses of honey bee colonies. NC1173 members are addressing the Varroa destructor mite challenge by developing novel chemical and biological control options for management (Johnson, OSU; Ellis, UF; Shepard, WSU), determining the seasonal efficacy of commonly used miticides (Ellis, UF), and examining management practices, including the use of screened bottom boards, that reduce mite populations (Huang, MI State). Williams (Auburn), Cook and Evans (USDA), and Delaplane (Georgia) collaborated to evaluate a new oxalic acid based-treatment, Aluen CAP, for Varroa mite management. This product is considered organic and will likely be compatible with use during nectar flow. It provides a 42-day continuous exposure of oxalic acid through honey bee interaction with cellulose matrix strips left in the hive draped over brood frames. Aluen CAP is produced by Cooperativo de Trabajo Abicola Pampero (Buenos Aires, Argentina). Both U.S. data and a registration partner will be needed in order to obtain a U.S. EPA registration. Oxalic acid vaporization is approved for use and the UF Team (Jack, Ellis) were involved in determining the doses required to control Varroa mite infestation, and Sagili (OSU) and is testing the efficacy of the recommended label dose for Varroa management in the northwestern US. These efforts, in conjunction with research aimed at identifying novel compounds with miticide properties, or novel ways to deliver existing miticides (Williams, Auburn; Cook, USDA) are important to limiting honey bee colony losses due to mite infestation. Toward the development of alternative mite limiting treatments, the Sheppard Lab (WSU) continued to breed a novel strain of Metarhizium fungus through multiple host generations for improvement as a biological control agent against Varroa mites and conducted outdoor studies comparing Metarhizium to oxalic acid treatment. Their results showed that the Metarhizum exhibited comparable control to this existing mite treatment, and therefore they submitted prepatent application. Notably, these chemical centered efforts are aligned with continued investigation of hygienic behavior (e.g., removal of mite infested brood) (Spivak, UM) and mite-biting behavior (Li-Barlay, OSU; Harpur, Purdue) and bee breeding programs centered around these traits (Objective 2), as well as promotion of integrated pest management programs (IPM) that promote monitoring for mites and treating when necessary. All of these efforts are needed to mitigate mite-associated honey bee colony losses. NC1173 members are examining the impact of pathogens on colony health and longevity (almonds-Flenniken, MT State; samples from 2015 US National Honey Bee Disease Survey – Grozinger, PSU). These efforts take into account the relative role of a variety of abiotic and biotic factors, including landscape, chemical exposure, and transmission between different bee species within insect communities (Wu-Smart, UNL, Hines, Grozinger, PSU; Flenniken MT State; Tarpy, NCSU; Rangel, TAMU). For example, Hines (PSU) investigated differential microsporidian infection levels by bee species and by habitat and Flenniken (MT State) examined relative prevalence and abundance of a virus in sympatric mining bees and honey bees. Likewise, NC1173 members from Penn State are examining inter-specific pathogen transmission between managed and wild bees with insect communities (López-Uribe, Hines, Grozinger). For example, López-Uribe (PSU) investigated prevalence in titers of honey bee viruses in wild bees in cucurbit systems and found that DWV is highly prevalent in wild bees but at very low titers (Jones et al 2021). Hines (PSU) investigated differential microsporidian infection levels by bee species and by habitat. In addition, López-Uribe (PSU) also found that DWV titers tend to be higher in feral than managed colonies, and similarly, immune gene expression is significantly upregulated in feral colonies (Hinshaw et al 2021). The team is also involved in virus discovery and monitoring (Lopez-Uribe PSU; Grozinger PSU) and demonstrated that facilitated viral transmission through injection (mimicking transmission by Varroa) shifted viral populations between DWV-A and -B and resulted in selection of specific viral genotypes (Grozinger PSU). In addition, several NC1173 members are involved in virus discovery and monitoring (Flenniken MT, State; Schroeder UMN; Lopez-Uribe PSU; Grozinger PSU; Tarpy, NCSU). NC1173 members are investigating honey bee antiviral defense mechanisms and the impact of putative immune stimulants, which are provided via supplemental feeding, on the outcome of infections. Honey bee antiviral responses include activation of canonical immune pathways (e.g., Toll, JAK/Stat), the heat shock response, and dsRNA-triggered mechanisms in limiting virus infections (e.g., RNAi and non-sequence specific dsRNA-triggered immune responses) (Flenniken MT State).The influence of nutrition (specifically phytosterols, protein and lipid ratios) on the outcome of pathogenic infections is an active research are in several NC1173 labs (i.e., Sagili OSU; Rangel, TAMU; Grozinger, PSU). Likewise several labs are examining the impact of putative immune stimulants that may reduce virus infection (i.e., thyme oil, propolis extracts, and fungal extracts) (Flenniken, MT State; Spivak, UM, and Sheppard, WSU).The Flenniken lab utilized laboratory-based studies to determine that honey bees infected with a panel of viruses including DWV and two model viruses (i.e., Flock House virus and Sindbis virus) that were fed 0.16 ppb thyme oil in sucrose syrup exhibited greater expression of key immune genes and reduced virus abundance (Parekh et al 2021). In contrast, in the same study bees that were fed the antifungal agent used to treat nosemosis (fumagillin) or sublethal doses of an insecticide (clothianidin) had reduced immune gene expression and higher viral loads compared to fed sucrose only diets. Together these results indicate that chemical stimulants and stressors impact the outcome of virus infection and immune gene expression in honey bees. This result was not unexpected, but it is important to quantitatively assess in order to potentially develop and promote management strategies aimed at boosting honey bee immune systems and reducing pathogenic infections. Along those lines, the UF team (Ellis) investigated how propolis extracts can be used to prevent and treat Vairimorpha (formerly Nosema) ceranae infection in honey bees and the Sheppard Lab (WSU) advanced testing of polypore mushroom extracts for use as a honey bee feed additive. In addition, the Sheppard lab carried out nutritional analysis of fungal extracts indicated that they contain a suite of minerals and other constituents that are similar to honey and pollen. This team completed an AAFCO requested longevity study comparing fungal extracts to honey and sugar syrup. WSU has coordinated with AAFCO and the FDA to seek a smooth and quick route to registration of the mushroom extract as a honey bee feed additive. Behavioral responses including the relationship between hygienic behavior and virus transmission are also under continued investigation (Spivak, UM). Likewise, the Rangel Lab (TAMU) is also examining the effects of self-removal behavior of workers in response to Varroa parasitization and/or other stressors (Rangel, TAMU). Members of the NC State Apiculture Program investigated vertical transmission of viruses and other pathogens from honey bee queens to their offspring (Rueppell & Tarpy, NCSU), and the horizontal transmission of viruses from workers to queens (Lee, Spivak, Schroeder, UM; Tarpy, NCSU). Further, Oregon State University team (Sagili and Melathopoulos) is examined the factors involved in high prevalence and intensity of European Foulbrood disease in honey bee colonies pollinating early season specialty crops such as blueberries. The Huang Lab (MSU) used cell invasion bioassays on a modified four-well arena, we showed that V. destructor significantly preferred to invade the worker and drone larvae of A. mellifera rather than A. cerana, suggesting that the new host is much more attractive to the parasite than the original one. Using gas chromatography-mass spectrometry (GC-MS), they revealed significant differences between the cuticular hydrocarbon (CHC) profiles of worker and drone larvae of the two bee hosts. A. mellifera worker and drone larvae were found to express significantly higher amounts of methyl-alkanes, while A. cerana larvae produced higher amounts of alkenes. Cell invasion bioassays with glass dummies showed that the mites preferred the glass dummies coated with the CHCs of A. mellifera worker or drone larvae, which indicates a role of larval CHCs in mediating the preferential cell invasion of Varroa. Short outcomes, Objective 1a: The strong association between Varroa destructor, deformed wing virus (DWV), and high overwintering colony losses (OCL) of honey bees is well established. Research indicates that increasing floral diversity in pollinator habitats reduces pathogen levels (Hines, Grozinger, PSU; Flenniken, MT State). Managed bee populations in the US have a greater diversity of viruses than previously realized (Grozinger, PSU) and virus infections at the colony level are dynamic, and thus longitudinal studies that precisely control sampling date are important to understand the impact of pathogens on honey bees at the colony level (Flenniken, MT State). At the molecular level, the heat shock stress response pathway is an important antiviral defense response to a model virus and chemical stimulants (0.16 ppb thyme oil) boost immune resonses and reduce virus infection levels, whereas chemical stressors have the opposite effects (Flenniken, MT State). Investigators at WSU are breeding a novel strain of Metarhizium fungus for improvement as a biological control agent against Varroa (Sheppard, WSU). The team conducted outdoor studies comparing Metarhizium to oxalic acid, a commonly utilized mite treatment, and showed that the Metarhizum exhibited comparable mite control (Sheppard, WSU). Additional testing (i.e., nutritional analysis) of polypore mushroom extracts for potential use as a honey bee feed additive were carried out and indicated that the extracts have a mineral composition similar to honey and pollen and an AAFCO requested longevity study was completed (Sheppard, WSU). The UF Team (Ellis) and colleagues demonstrated the feeding honey bees propolis extracts can reduce V. ceranae spore counts and, in some cases, help prevent infection in adult honey bees. They (Jack, Ellis) also determined that the labeled rate for oxalic acid vaporization is insufficient to control Varroa in managed honey bee colonies. They found that the dose needed for effective Varroa control is higher than that labeled for use. This recent finding may inform a label change for oxalic acid. Outputs Objective 1a: NC1173 published numerous peer-reviewed publications related to pest and pathogen stressors, which are listed at the end of this report; many of them are open-access. A USDA APHIS PPQ grant was secured to continue investigation into landscape factors driving wild bee pathogen levels in another region (North Carolina), which, together with Pennsylvania data, will help refine best management practices for promoting healthy bees (Hines, Grozinger, PSU). Ongoing studies of pathogen dynamics of wild and managed bees in cucurbit systems (López-Uribe PSU) will shed light on the role of managed pollinators as reservoirs of pathogens that can be transmitted to wild bees. López-Uribe was awarded a USDA-NIFA Pollinator Health grant to work on the interactions between biotic and abiotic stressors under climate change. Via a meta-analysis, Williams (Auburn) found that antagonistic interactions between pesticides and parasites appear to be overlooked by the scientific community. The UF Team (Jack, Ellis) tested new compounds for efficacy against Varroa and safety for honey bees. They found a promising new treatment for Varroa that they plan to move into Phase 2 testing in future project reporting periods. Furthermore, they continue to screen for additional compounds that can be used to control the mite. Objective 1b: (Abiotic Stressors: Pesticides, Forage Availability, Nutrition) Major abiotic stressors contributing to honey bee health decline include pesticide exposure and malnutrition. NC1173 members are addressing these factors through studies examining the pesticide residue levels found in bee forage (floral nectar and pollen) in ornamental plants treated with systemic insecticides (Eitzer, Stoner, and Cowles, NC1173 members are examining  the levels of pesticide residues in pollen from honey bees and floral resources in relation to the pesticides applied by growers in Northeastern pollinator-dependent crops (Eitzer, Stoner, CAES; Averill, U Mass), examining the pesticide residue levels found in bee forage in urban areas (Rangel, TAMU; Huang, MI State; Ellis, UF), examining the role existing tree lines play as drift barriers to reduce off-target contamination from neonicotinoid-laden dust released during corn planting into forbs growing near corn fields (Wu-Smart, UNL), examining which plants bees are utilizing in natural landscapes and in open spaces near agricultural crops (Kim, Speisman, KSU; Wu-Smart, UNL; Johnson, Ohio State), and the microbial (bacterial and fungal) communities in bee forage (Danforth, Cornell) to better understand the nutritional requirements of managed and wild bees (Osmia cornifrons (Megachilidae)) and the role fungicides play on these microbes. As described above, the Flenniken lab carried out caged based studies to quantify the impact of a beekeeper applied fungicide (fumagillin) and sublethal doses of clothianidin on virus infection and suppression of immune gene expression. Further, some of these issues with pesticide exposure, malnutrition, and/or pollination deficits/limitations are being examined in specific cropping systems (apples-Danforth, Cornell; black cherry-Hoover & Grozinger, PSU; corn/soybeans-Wu-Smart, UNL). In addition, are working to assess the potential toxicity of pesticides and spray adjuvants to various honey bee life stages and characterize risks associated with exposure to these compounds (Jack and Ellis, UF; Johnson, Ohio State). Williams (Auburn) demonstrated negative effects of the next-generation pesticide, flupyradifurone, on honey bee behavior and survival, while his other work revealed effects of neonicotinoids on bumble bee, but not orchard bee, physiology. Winfree (Rutgers) has published results showing that many crops, and especially spring-blooming fruit crops, are pollination-limited in the USA (Reilly et al 2020). Ongoing work includes identification of the main flowering plant species used as pollen sources by spring-flying native bee species such as Andrena and Osmia, which are important pollinators of spring tree fruit (Winfree, Rutgers). Knowledge of pesticide stressors on pollinators has been incorporated into crop integrated pest management programs to reduce pollinator exposure to pesticides at critical times of the crop production season. Integrated Pest and Pollinator Management systematizes this practice and should be considered in all insect-pollinated crops (Biddinger and Rajotte, PSU, Joshi UArk). Penn State NC1173 Grozinger and Patch members evaluated the attraction of pollinators to 20 ornamental perennial plant species and cultivars and used network theory to identify the most important species (Erickson et al 2021). They demonstrated that successional forests and clearings in forests support more floral diversity and more pollinators (Mathis et al 2021 and Lee et al 2021).  Moreover, the protein:lipid ratio of pollen-based diets significantly influences resilience to pesticide exposure (Crone et al 2021). Grozinger and Patch (PSU) also investigated the economic value of pollination services in the US and demonstrated that the economic value dependent on pollination service totals 34.0 billion USD in 2012, considerably higher than previous estimates. PSU NC1173 members also evaluated the impacts of land use, habitat, weather and climate on wild bee communities in the mid-Atlantic states and on honey bee winter survival in Pennsylvania and demonstrated that weather conditions in previous seasons were primary drivers of wild bee diversity and abundance and honey bee winter survival (Kammerer et al 2021 and Calovi et al 2021). In addition, the PSU team secured funding to develop resources to improve pollen diagnostic abilities by developing a streamlined metabarcoding pipeline (Grozinger) and pollen image library (Boyle) (Funding from PA Dept of Agriculture). Honey bee exposure to pesticides in urban environments (Rangel, TAMU; Huang, MI State; Ellis, UF) These NC1173 members conducted a nationwide study focused on characterizing honey bee exposure to pesticides in nectar and pollen collected in urban settings. Furthermore, they performed a risk assessment using the US EPA’s BeeREX model when oral toxicity values were available for compounds discovered in the pesticide screen. The screen identified 17 different pesticides in nectar and 60 in pollen. Most of the samples (~73%) contained no pesticide residues. Using BeeREX, the team demonstrated that four insecticides showed a potential acute risk to honey bees (imidacloprid, chlorpyrifos and esfenvalerate in nectar, and deltamethrin in nectar and pollen). Nevertheless, exposure of honey bees to pesticides via nectar and pollen was low in the sampled urban areas. The Spiesman lab at Kansas State University conducted wild bee visitation surveys in tallgrass prairie landscapes across eastern Kansas. Our goals are to understand how climate variability affects variability in interaction network structure. Sample processing is underway, and results will be known in August 2022. Efforts by Eitzer, Stoner, Cowles (Conn) include the establishment of high-yielding floral resources plots. These plots will be used to support honey bee genetic improvement programs, and also to enhance landscapes to support a broad diversity of pollinators.  They plan to obtain quantitative data on honey yield from hives using these plots which could spur their acceptance in fixed-land honey crops.  To date 10 of 12 planned species have been established on these plots.  Methods to establish these plants are described in this video:  <a href="https://www.youtube.com/watch?v=rzyEyNf5CaU">https://www.youtube.com/watch?v=rzyEyNf5CaU</a> . Of the species planted, the hairy mountain mint and narrow-leaved mountain mints have had the best combination of being the most attractive (and presumably having the highest yield of nectar) and easiest to establish in solid stands.  Species that were unsatisfactory have been lemon balm (mostly attractive to wool carder bees) and Scrophularia marylandica, which does not appear to be especially attractive. Building the first pollen nutrition database for bee pollinators in North America (Ramesh Sagili, OSU and Priya Chakrabarti Basu, MSU): The research team was recently funded with a $500,000 grant from USDA-AFRI to collect pollen from 100 major bee-pollinated plants across North America and analyze the nutritional content of their pollens. The project team has partnered with NRCS, USDA and USGS, in additional to large pool of citizen scientists in USA and Canada for pollen collections. Pollen lipids, proteins, phytosterols and amino acids will be analyzed and the database will be publicly available for researchers, policy makers, citizens and stakeholders. The results will also be published in peer-reviewed journals. Currently in addition to the PI and co-PI, there are two graduate students working in this project. NC1173 members from Oregon State (Sagili Honey Bee Lab) and Mississippi State (Chakrabarti Honey Bee Lab) are also working on investigating the role of varying concentrations of 24-methylenehcolesterol (an important micronutrient) on honey bee colony health and physiology. In addition, they are also investigating the impacts of sterol biosynthesis inhibitory fungicides on honey bees and plant pollen sterol nutritional quality The MSU Bee Lab (PD Chakrabarti) is newly established and is currently recruiting graduate students to work on projects related to pesticide toxicity, nutrition, climate change and interaction of multiple stressors on bee pollinators. PD Chakrabarti is currently building collaborations with stakeholders across Mississippi and is also in the process of establishing a research apiary on main campus at MSU. NC1173 members in the NC State Apiculture Program investigated the effects of abiotic stressors (temperature and pesticides) on honey bee queens and particularly their reproductive quality (Pettis, Tarpy). They determined the thermal limits to sperm survival in queen spermathecae (sperm storage organs) as well the proteomic changes in queens as a consequence of temperature and pesticide exposures. The Connecticut Agricultural Experiment Station team (Eitzer, Stoner, Cowles) collected trapped pollen from honey bee colonies in different environments (ornamental plant nurseries and botanical gardens) and are analyzing the plant sources of the pollen and the pesticide residues found in the pollen. The plant sources were analyzed using palynology (identification of acetolyzed pollen using light microscopy) and by DNA metabarcoding (contracting with researchers at the University of Maine and Ohio State University, respectively). The pesticide residues are extracted using a version of the QuEChERS protocol and then analyzed using liquid chromatography/mass spectrometry (contracting with researchers the US Department of Agriculture) and gas chromatography and mass spectrometry (US Department of Agriculture). They are comparing the results of the two methods of plant identification and relating the plant sources of the pollen to the pesticide residues found. Chronic and persistent bee losses occurring in Mead NE uncovered an improper method of disposing pesticide treated crop seeds through ethanol production. The disposal practice resulted in high concentrations of pesticide-laden waste byproducts which were land applied as soil conditioners without farmers’ knowledge of pesticide contamination loads. Soil samples taken 2+ years after land application of contaminated waste byproducts (also known as distiller’s grains or wetcake) exhibited high pesticide loads, including systemic pesticides, such as neonicotinoid insecticides (clothianidin (average 7579 ppb; high 24,615 ppb; n=6) and thiamethoxam (average 3569 ppb; high 12,241 ppb; n=6)) and several strobin- and azole- type fungicides (fluoxastrobin (average 5770; high 16,650; n=6) and tebuconazole (average 16,555; high 38,595; n=6). Pesticide residues at these levels would be harmful to bees particularly ground nesting bees as well as when pesticide residues are translocated into non-target pollinator-friendly plants. The UNL Bee Lab recruited the Mead Pollution Research team (~13+ University of Nebraska Medical Center, University of Nebraska-Lincoln, & Creighton University researchers) and secured gap funds to support field sampling of vegetation, soil, and water in 2021. Received NC1173 Multistate project funds ($150,000; 3-yrs) to begin the One Health Student Internship with Dr. Liz Van Wormer (co-PI). This program seeks to mentor a cohort of undergraduates to work collaboratively across disciplines and along researchers seeking to collect environmental and ecological samples and conduct investigations into potential impacts caused by AltEn pollution. UNL Bee Lab sampled wildflowers, trapped pollen, and in-hive food stores to investigate the potential route(s) of pesticide exposure for honey bee colonies impacted by AltEn pollution. Pesticide analyses of plants and in-hive samples are being conducted by Drs. Michelle Hladik (USGS-CA) and Dan Snow (NE Water Science Lab). Protein/lipid analyses of field collected plants, in-hive pollen stores, and brood jelly will be conducted by NC1173 member Dr. Chakrabarti Basu (Mississippi State University) to assess potential degradation of food quality. In addition to collecting environmental samples for pesticide testing, sentinel hives and observation hives were placed on site to assess impact to colony development, age-polyethism or division of behavioral hive tasks, and queen rearing capabilities. In addition, The Danforth lab (Cornell) conducted a series of experiments to determine how widely-used fungicides (Difenoconazole and Captan) impacts larval development in a common, easily-manipulated, mason bee (Osmia cornifrons; Megachilidae). They developed two experiments to specifically determine how fungicides impact the normal progression of larval development and whether the fungicidal treatments impacted the microbial community of the pollen provisions upon which these larvae are feeding. In addition, the TAMU bee lab (Rangel, Texas A&M University) wrapped up a project looking at the effects of pesticide exposure on honey bee queen and drone reproductive health. They looked at whether exposure of queen and drone larvae to wax contaminated with field relevant concentrations of miticides and agro-chemicals affected sperm count and viability, size, queen egg-laying capacity, chemical composition of queen mandibular gland pheromones, and ovariole size. The Johnson lab (Ohio State) explored the effects of bloom-time pesticide applications made to almonds on honey bee worker adults and larval queens and workers.  They assessed the toxicity of insecticide-fungicide combinations and the effect of spray adjuvants, alone and in combination with pesticide tank-mix partners on honey bee survival. The Huang Lab (MSU) continued to examine transportation stress on honey bees. They  determined gene expression in bees that were “transported” (shaken in a lab for 6 days) and control (not shaken). They are interested in determining whether transported bees would down regulate their detoxification genes because a previous unpublished study showed shaken bees were more sensitive to pesticides. They determined the gene expression of bees in both shaken and unshaken bees for two P450 genes, c305, C6BE, GST (glutathione S-transferase), and defensin (a gene encoding an antimicrobial peptide) and two reference genes (actin and GADPH). Contrary to their prediction, they did not find reduced gene expression in the transported group (and one gene (i.e., c305) exhibited increased expression). They are continuing to explore this line of investigation. Short outcomes, Objective 1b: The PSU team, (1) demonstrated that ornamental plant species can serve as important forage resources for managed and wild bees, but there is considerable variation among cultivars (2) early successional forests and clearing significantly improve pollinator abundance in forest systems (3) identified the optimal protein:lipid ratios of honey bee diets to support resilience to pesticides (4) found that weather in previous seasons strongly influenced wild bee abundance and diversity and honey bee colony winter survival  (5) showed that economic value of insect pollination services to agricultural systems in the US is considerably higher than previous calculated Likewise, research teams including Rangel (TAMU), Huang (MI State) and Ellis (UF) analyzed the pesticides present in nectar and pollen samples in urban and suburban areas across the U.S. The resulting manuscript has been accepted and will be published during the next project reporting period. Williams (Auburn, AL) and team observed that antagonistic interactions between parasites and pesticides are common in honey bees. Stoner (CAES, in collaboration with US EPA, U Maine, UMD) has found major gaps in the ability of commonly used DNA metabarcoding methods to detect, much less quantify, pollen collected by honey bees from maize and buckwheat in mixed pollen samples. This calls into question much research relying solely on metabarcoding for pollen analysis without cross-referencing to microscopic palynology. Lastly, the insights gleaned from the studies carried out at Oregon State University on honey bee nutrition have advanced the understanding of sterol metabolism and regulation in honey bees and will assist in formulation of a more complete artificial diet for honey bees (Sagili and Chakrabarti). Tests of tank-mix pesticide combinations have identified a subset of spray adjuvants that are both toxic at field-relevant concentrations and were made more toxic when mixed with pesticides (Johnson). Outputs, Objective 1b: NC1173 member (Grozinger, PSU) worked with collaborator Anthony Robinson to evaluate the utility of the Beescape portal for beekeepers and identified strategies to improve the usability and value of the portal. Given the severity of the systemic pesticide pollution issue occurring in NE and unclear alternatives for proper safe disposal of treated crop seeds, NC1173 member Wu-Smart has engaged with community leaders, legislators, and advocates which has led to legislative actions at the local level: NE bill <a href="https://nebraskalegislature.gov/FloorDocs/107/PDF/Intro/LB507.pdf">LB507</a> The Ethanol Development Act, “in which the use of treated seed corn in the production of agricultural ethyl alcohol shall be prohibited if such use results in the generation of a byproduct that is deemed unsafe for livestock consumption or land application”, (<a href="https://drive.google.com/file/d/11zfQSB3GqhjXLo7tDHxRSkK-5OW7Dkcc/view?usp=sharing">testimony</a> Feb 3, 2021); NE bill <a href="https://nebraskalegislature.gov/FloorDocs/107/PDF/Intro/LB634.pdf">LB634</a> which seeks to provide a cause of action for unsafe disposal of treated seed (<a href="https://drive.google.com/file/d/167ipo1mjlwTsEMEMMKQZ0lsJyMdWdypu/view?usp=sharing">testimony</a> March 10, 2021); and MN bill <a href="https://www.revisor.mn.gov/bills/bill.php?b=House&f=HF0766&ssn=0&y=2021">HF766</a> a type of “extended producer responsibility” bill introduced by MN Representative Rick Hansen (District 52A) that seeks better product stewardship and accountability from producers (<a href="https://drive.google.com/file/d/1lCqalZco_5Z-nyZ6J7k2HSx2Sttnq9p7/view?usp=sharing">testimony</a> March 22, 2021). In these testimonies, information was provided that highlighted critical needs to examine and regulate treated seed practices to better control and manage systemic pesticide pollution. Conducted interviews and discussions with NJ Assemblyman Clinton Calabrese regarding NJ Bill <a href="https://www.njleg.state.nj.us/bill-search/2020/A2070">A2070</a> which prohibits most outdoor non-agricultural uses of neonicotinoids (passed Jan 2022). Objective 2: (Genetics, Breeding, & Diversity) Breeding mite and disease resistant traits in honey bee stock and diversifying honey bee genetics and selection efforts are more sustainable solutions to address the pest and pathogen issues in honey bees and is a long-term goal for NC1173 members. Efforts include studies to examine how establishing high-yield nectar crops support high densities of honey bee colonies required for mating yards in honey bee genetic improvement programs (Eitzer, Stoner, Cowles -CAES; Harpur Purdue University) and breeding and selection of high grooming/mite biting behavior in Ohio feral colonies (Li-Byarlay, CSU).  Sheppard and the WSU team continued selection and maintenance of the New World Carniolan strain of honey bee, including inputs of cryopreserved A. m. carnica germplasm from Slovenia origin.  They produced and supplied instrumentally inseminated (i. i.) “breeder” queens to a number of commercial queen producers of open-mated NWC “production” queens. Together with industry partners, in 2021 WSU handed off the production of i. i. New World Carniolan i. i. breeder queens to commercial queen producer.  Starting in 2021, NWC breeder queens supplied to the queen production industry came from queen producer partners (rather than WSU).  WSU continued to be responsible for maintenance of the genetic stocks and infusion of A. m. carnica genetics from our repository of cryopreserved Old World semen.  In addition, the WSU team continued selection and distribution of a Caucasian strain of honey bees derived from Old World origins.  Using cryopreserved semen from collections of A. m. caucasica germplasm made over the past decade in the country of Georgia, WSU continues its effort to reintroduce this strain of honey bee to US beekeepers. In 2021, they supplied i.i. breeder queens to a number of commercial queen producers, who produced open-mated daughters for sale throughout the US.  This strain is especially interesting to beekeepers from colder climates within the US. Spivak and UM team initiated a new bee breeding program in 2019 to understand mechanisms of resistance to Varroa mites and diseases.  They evaluate treated-parent colonies and untreated-daughter colonies for wintering survivorship 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).  Untreated colonies that survive winter are used as breeding stock the following summer. Parent colonies of the survivors are evaluated and sampled for future evaluation of ‘omic pattern associated with resistance.   The Huang Lab (MSU) identified three genes for mushroom body large-type Kenyon cell-specific protein-1 (Mblk-1) encodes a putative transcription factor and is expressed preferentially in the large-type Kenyon cells of honey bee mushroom body. Mblk-1 is thought to be involved in brain function by regulating transcription of its target genes, however its function in the honey bees is obscure. They showed that Mblk-1 had significantly higher expression in the brains of forager bees relative to nurse bees regardless of their age. Inhibition of Mblk-1 decreased sucrose responsiveness in foragers. Finally, we determined that Mblk-1 indirectly targets the mRNA of gustatory receptors. These findings suggest that Mblk-1 plays important roles in regulating honey bee division of labor. Short outcomes, Objective 2: Purdue University (Harpur) breeding program with mite resistant traits has been successfully made available in ten US States. The Purdue team is currently exploring integrating genomic selection and genetics into breeding decisions and they have developed international collaborations (Gregor Gorjanc; Rosalind Institute) to begin developing theory and empirical data to incorporate genomics into bee breeding. Harpur is funded by the Eva Crane Trust) to explore the genetic diversity of honey bees across the United States to understand baseline levels of genetic diversity. Harpur and Lopez-Uribe secured a USDA AFRI (USDA AFRI 102265) to determine how different honey bee genetic lines perform in the hands of beekeepers. Harpur (Purdue) and Lopez-Uribe (PSU) received a USDA-CARE grant to compare the performance of different honey bee stocks in different regions of the MidAtlantic. The project involves the participation of 30 beekeepers in IN and PA. Grozinger and Rasgon are developing tools for genetic manipulation/transformation of bees (Penn State), which will facilitate the identification and validation of genetic markers for bee health and behavior; this project is funded by the NSF-EDGE program. Genomic studies by Patch and collaborators demonstrated that honey bees likely originated in Asia and identified genomic “hotspots” for supporting adaptive radiation in subspecies. With funding from the Pennsylvania Department of Ag, López-Uribe and Harpur are sequencing the genomes of feral colonies and several genetic stocks to estimate levels of Africanization in colonies in the northeast of the US. With funding from an NSF-CAREER award, López-Uribe is investigating the evolutionary responses of bees’ sensory systems to the domestication of flowers in crops. Spivak (UM) is funded by USDA AFRI (2018-67013-2753) to conduct a multi-trait breeding program for mite resistance (described above). NC1173 members (Ellis, UF) are working with collaborators to develop a stock certification program for honey bees in Puerto Rico. Outputs, Objective 2: NC1173 members worked directly with over numerous beekeepers and nearly through extension programs and courses, which were mostly virtual in 2021. Penn State offered a winter webinar series that was attended by at least 3,000 beekeepers from all over the US. Harpur (Purdue) provides Varroa-resistant stock (Indiana Mite biters) to beekeepers across 10 States, and researchers (Li-Byarlay, CSU; Lopez-Uribe PSU). Central State University provided extension talks to 600+ beekeepers and general public including extension webinars at CSU, talks at national bee conferences, one scientific publication on mite biting behavior and mite-resistance published in Frontiers in Ecology and Evolution (Smith et al, CSU). Flenniken, Sagili, and other NC1173 Members gave presentations to the Bee Informed Tech Transfer team and numerous beekeeping organizations (e.g., California State Beekeepers Association, Montana State Beekeepers Association, Southwest Ohio Beekeeping Club (with over 200 attendees online)). Spivak lab delivered over 50 talks to over 5000 beekeepers locally, nationally and internationally. Dr. Walter S. Sheppard (WSU) completed the Video - Honey Bee Breeding and Practical Selection Methods, which has received more than 8.2K views, including national and international audiences. The video was awarded a Bronze Award for Educational Video from the Association of Natural Resource Extension Professionals and has been shown in numerous classrooms. It is also featured in a Podcast discussion, Beekeeping Today Podcast, presented by Bee Culture Magazine.  Links to the video and podcast are available on line: Video on Selection Methods and Honey Bee Breeding, YouTube: <a href="https://youtu.be/R8-9DgXcrfI">https://youtu.be/R8-9DgXcrfI</a> and Vimeo: https://vimeo.com/380776410. Objective 3: (Management) Management practices to maintain healthy honey bees and landscapes that support pollinators are in high demand and recommendations continue to evolve with new research. Therefore, NC1173 members strive to engage with stakeholders to better provide the most up-to-date, science-based recommendations to beekeepers, pesticide applicators, farmers, homeowners and policy makers. Recommendations include how to better manage pests and pathogens in honey bees(especially concerning the Varroa mite (Williams, Auburn), enhancing landscapes for pollinators, and options to reduce exposure or mitigate effects of pesticides. NC1173 members gave presentations to numerous stakeholder groups (highlighted in other section), and Harpur (Purdue) created a digital seminar series for beekeepers called “Winter Cluster” and provided training to bee breeders on Instrumental Insemination and Queen Rearing. Through a USDA-OREI funded project, López-Uribe and Underwood successfully developed a sustainable and economically profitable protocol to incorporate organic management practices into beekeeping. NC1173 members conducted studies to identify the most attractive and nutritionally beneficial species of plants in urban (Erickson et al 2021) and forest settings (Mathis et al 2021, Lee et al 2021). NC1173 members (McLaughlin, Hoover and Grozinger PSU) conducted studies in Spring 2020 to define the pollinator communities for black cherry, a key timber species in northeastern forests suffering from declining regeneration, and the environmental factors that influence pollinator abundance and diversity. Using a combination of passive and active sampling techniques, pollinators were collected from flowering black cherry trees in the Allegheny National Forest and in State College, PA. PSU team members analyzed pollen macronutrients from 82 plant species and collected pollen from three bee species to demonstrate that there is considerable variation in the protein:lipid ratios, thus potentially allowing us to select plants that provide optimal nutrition for different bee species (Grozinger, Patch, Hines). Central State University in Ohio held workshops in a combination of online and in person for improve diversity of queen bees by distributing 48-hour queen cells for local beekeepers. CSU plans to do future trainings on workshops to Ohio beekeepers on how to do grafting and queen rearing for genetic diversity and breeding. Potter et al. (University of Kentucky) completed and published a multi-year study of alternative lawns consisting of dwarf varieties of white clover (Trifolium repens) in pure stands or intermixed with turfgrass.   Dwarf clovers have been selected for small leaf size and low growth habit, allowing them to tolerate low mowing heights and blend better with lawn grasses. The study showed that the dwarf clovers augment nitrogen and resist white grubs, reducing need for fertilizer and insecticide inputs, and support both honey bees and diverse assemblages of wild bees similar to those that visit conventional white clover.  The CAES team (Stoner, Zarrillo) initiated studies on the pollinator community of chestnut, Castanea spp., working with volunteers from the American Chestnut Foundation and utilizing the diverse collection of chestnut species, inter-species crosses, and cultivars, a product of over 100 years of chestnut breeding efforts, at our experimental farm. The Huang Lab (MSU) examined mechanisms of floral attraction to honey bees and determined the nectar production of two varieties of Bidens, Portulaca, and Tagetes. One that was highly attractive to honey bees and one not in each plant. They found significantly higher nectar production in the more attractive variety in Bidens and Portulaca, but we failed to obtain measurable nectar in either variety of Tagetes. The Spivak Lab (UM) concluded a study on the establishment and benefit of “Bee Lawns,” which was funded by the Minnesota Environmental and Natural Resources Trust Fund and determined that there is increased interest in enhancing areas dedicated to lawns using flowering species to support pollinators. They intentionally introduced low-growing flowers to turfgrass lawns to promote bee diversity and reduce inputs, while maintaining the traditional aesthetics and recreational uses associated with lawns. They found that Kentucky bluegrass and hard fescue are promising turf companion grasses for future forb/turf inter-seeding. Of the eight forbs tested, Trifolium repens L., Prunella vulgaris ssp. lanceolata, Thymus serpyllum auct. non L., and Astragalus crassicarpus Nutt. were most promising. In the bee lawns established in Minneapolis parks, they found 56 species of bees on T. repens, with A. mellifera as the most common species observed. Florally enhanced lawns supported more diverse bee communities than lawns with just T. repens, and the bee communities supported by florally enhanced lawns were significantly different from the bee communities supported by lawns containing just T. repens. 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. Short outcomes, Objective 3: With funding from the PA Department of Ag, López-Uribe is leading a statewide bee monitoring project through participatory science with Master Gardeners. Williams (Auburn, AL) performed a citizen science experiment that examined effectiveness of different beekeeper learning types concerning Varroa, and performed several experiments to identify novel active ingredients or management actions against the mite. Sagili (OSU) synthesized a Survey-derived best beekeeping management practices to improve colony health and reduce mortality. These studies related to honey bee colony management provide additional tools/practical methods for beekeepers to enhance colony health and survival. Outputs, Objective 3: PA Bee Monitoring Program: López-Uribe is working in collaboration with Penn State Extension and Master Gardeners on a statewide bee monitoring project. The goals of the project are to increase knowledge of bee diversity across Pennsylvania and to collect long-term data to detect changes in abundance and species composition over time. Harpur (Purdue) - The cluster brought in beekeepers, researchers, and extension specialists from around the world and hosted over 300 people. We focused on topics related to Varroa treatment, winterizing colonies, Fall garden management for bees, and youth beekeeping. Our Instrumental Insemination and Queen Rearing course trained 30 people from across the US. We are expanding these courses by providing them in a digital format in 2022.  Potter (University of Kentucky) delivered virtual lectures on “Bees, Pesticides, and Politics: Challenges and Opportunities Sustainable Urban Landscapes” at major 2021 conferences and venues attended by thousands of stakeholders (e.g., American Hort national webinar, Conn. Native Plants and Pollinators Conf., Illinois Green Industry Conf., Alabama “Raising Trees” webinar series, Michigan Green Industry Assoc., NC State Master Gardeners/Extension Agents, Ohio State Univ. Landscape and Turf webinar, KY Pollinator Stakeholder group, Green & Growing Atlanta, and others). Stoner (CAES) provides technical assistance to the Pollinator Pathway  network (<a href="https://www.pollinator-pathway.org/">https://www.pollinator-pathway.org/</a>), which organizes diverse stakeholders (including environmental organizations, land trusts, garden clubs, municipal governments and other community groups) to encourage planting native plants attractive to pollinators and reducing or eliminating pesticide use. This organization, which started in southwest CT, now stretches throughout New England, New Jersey, eastern New York and Pennsylvania, and down the East Coast to Maryland. Over 70 towns (out of 169 total) in Connecticut alone now have active Pollinator Pathway programs.

Publications

Summary table and list of publications by topic reported by NC1173 committee members for 2020. NC1173 authors are indicated in bold. <table width="557"> <tbody> <tr> <td width="461"> Publications by topic </td> <td width="96"> 2021 </td> </tr> <tr> <td width="461"> Obj 1a: Biotic (Pests & pathogens) </td> <td width="96"> 25 </td> </tr> <tr> <td width="461"> Obj 1b: Abiotic (Pesticides, nutrition, landscapes) </td> <td width="96"> 32 </td> </tr> <tr> <td width="461"> Obj 2: Genetics, Breeding, Diversity </td> <td width="96"> 17 </td> </tr> <tr> <td width="461"> Obj 3: Management </td> <td width="96"> 14 </td> </tr> <tr> <td width="461"> Other Publications </td> <td width="96"> 5 </td> </tr> <tr> <td width="461"> Total </td> <td width="96"> 93 </td> </tr> <tr> <td width="461"> Publications with >1 NC1173 authors </td> <td width="96"> 12 </td> </tr> </tbody> </table>   NC1173 Member Publications (01/01/2021 to 12/31/2021) *Papers applicable to multiple objectives are only reported once. Wu-Smart J, Kittle S., Couvillon, M., López-Uribe, M. 2021. Proceedings of the 2021 American Bee Research Conference. Bee Culture (March edition) pp 46-58. Objective 1a: Biotic Stressors (Pests & pathogens) Naree, S., Benbow, M.E., Suwannapong, G., Ellis, J.D. 2021. Mitigating Nosema ceranae infection in western honey bee (Apis mellifera) workers using propolis collected from honey bee and stingless bee (Tetrigona apicalis) hives. Journal of Invertebrate Pathology, 185: 107666, 8 pgs. https://doi.org/10.1016/j.jip.2021.107666. Jack, C.J., van Santen, E., Ellis, J.D. 2021. Determining the dose of oxalic acid applied via vaporization needed for the control of the honey bee (Apis mellifera) pest Varroa destructor. Journal of Apicultural Research, 60(3): 414 – 420. https://doi.org/10.1080/00218839.2021.1877447. Hinshaw C, Evans KC, Rosa C, López-Uribe MM. (2021) The role of pathogen dynamics and immune gene expression in the survival of feral honey bees. Frontiers in Ecology and Evolution 8: 505. Jones LJ, Ford RP, Schilder RJ, López-Uribe MM. (2021) Honey bee viruses are highly prevalent but at low intensities in wild pollinators of cucurbit agroecosystems. Journal of Invertebrate Pathology 185: 107667, Ray, A. M., Davis, S. L., Rasgon, J.L. and C.M. Grozinger. Simulated vector transmission differentially influences dynamics of two viral variants of deformed wing virus in honey bees (Apis mellifera). Journal of General Virology 102(11):001687 https://doi.org/10.1099/jgv.0.001687 (2021). Williams, M.-K., Cleary, D., Tripodi, A., Szalanski, A. L. (2021). Co-occurrence of Lotmaria passim and Nosema ceranae in honey bees (Apis mellifera L.) from the United States. Journal of Apicultural Research. 10.1080/00218839.2021.1960745. Faber N.R., Meiborg A.B., McFarlane G.R., Gorjanc G., & Harpur B.A. (2021). A gene drive does not spread easily in populations of the honey bee parasite Varroa destructor. Apidologie. DOI:10.1007/s13592-021-00891-5. Wen X, Ma C, Sun M, Wang Y, Xue X, Chen J, Song W, Li-Byarlay H, Luo S, 2021, Pesticide residues in the pollen and nectar of oilseed rape (Brassica napus L.) and their hazards to honey bees.  Science of The Total Environment, 786, 2021,147443, https://doi.org/10.1016/j.scitotenv.2021.147443. Swami, R., B. Gasner, D. R. Tarpy, M. K. Strand, O. Rueppell, and H. Li-Byarlay. (2021). Assessment of two different extraction methods on nucleic acids for sociogenomics. Annals of the Entomological Society of America, 114: 614–619. Bird, G., Wilson, A.E., Williams, G.R., Hardy, N.B. 2021. Parasites and pesticides act antagonistically on honey bee health. Journal of Applied Ecology 58, 997-1005. Sanchez, S., Shapiro, D., Williams, G.R., Lawrence, K. 2021. Entomopathogenic nematode management of small hive beetles (Aethina tumida) in three native Alabama soils under low moisture conditions. Journal of Nematology 53, e2021-63 Papach, A., Cappa, F., Cervo, R., Dapporto, L., Balusu, R. Williams, G.R., Neumann, P. 2021. Cuticular hydrocarbon profile of parasitic beetles, Aethina tumida (Coleoptera: Nitidulidae). Insects 12, 751. 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. 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. 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. Spivak M, Danka RG. 2020. Perspectives on hygienic behavior in Apis mellifera and other social insects.  Apidologie DOI: 10.1007/s13592-020-00784-z. 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. Spivak M, Cariveau DP. 2020. Flowers as parasite transmission hubs. Nat Ecol Evol. <a href="https://doi.org/10.1038/s41559-020-1200-z">https://doi.org/10.1038/s41559-020-1200-z</a> 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. <a href="https://doi.org/10.1371/journal.pone.0245490">https://doi.org/10.1371/journal.pone.0245490</a>. Li, W, Y. Zhanga, H. Peng, R. Zhang, Z. Wang, Z.Y. Huang, Y.P. Chen and Richou Han. 2021.  The cell invasion preference of Varroa destructor between the original and new honey bee hosts.  Internal J of Parasitology <a href="https://doi.org/10.1016/j.ijpara.2021.08.001">https://doi.org/10.1016/j.ijpara.2021.08.001</a>. Ma, Z., Y. Wang, Z.Y. Huang, S. Cheng, J. Xu, Z. Zhou. 2021. Isolation of protein-free chitin spore coats of Nosema ceranae and its application to screen the interactive spore wall proteins. Arch Microbiol.  <a href="https://doi.org/10.1007/s00203-021-02214-9">https://doi.org/10.1007/s00203-021-02214-9</a>. McMenamin, A.J., Brutscher, L., Daughenbaugh, K.F., and Flenniken, M.L., The honey bee gene bee antiviral protein-1 (bap1) is a taxonomically restricted antiviral immune gene, (2021), Frontiers in Insect Science, (2021) https://doi.org/10.3389/finsc.2021.749781. McMenamin, A.J.*, Parekh, F.*, Lawrence, V., and Flenniken, M.L., Investigating Virus-Host Interactions in Cultured Primary Honey Bee Cells, (2021), Insects,12(7):653; doi:10.3390/insects12070653. Parekh, F., McMenamin A.J., Daughenbaugh, K.F., and Flenniken, M.L., Chemical stimulants and stressors impact the outcome of virus infection and immune gene expression in honey bees (Apis mellifera), (2021), Frontiers in Immunology, (2021), https://doi.org/10.3389/fimmu.2021.747848. Han, J. O., Naeger, N.L., Hopkins B. K., Sumerlin D., Stamets P. E., Carris, L. M., and Sheppard,, W. S. <ol start="2021"> <li>Directed evolution of Metarhizium fungus improves its biocontrol efficacy against Varroa mites in honey bee colonies. Scientific Reports, v. 11, doi.org/10.1038/s41598-021-89811-2.</li> </ol> Hopkins, B.K., Long, J. Sheppard, W.S.  Comparison of indoor (refrigerated) vs. outdoor winter storage of commercial honey bee (Apis mellifera) colonies in the Western US.  J. Econ. Entomol. Accepted - in press.   Objective 1b: Abiotic Stressors (Pesticides, nutrition, landscapes) Lamke, K., Wedin D., and Wu-Smart, J. (accepted Jan 2022). Remnant prairies and high-diversity restorations support wild bees season-long. The Prairie Naturalist Journal Special Edition Ghisbain GM, Gerard TJ, Wood, Hines HM, Michez D. 2021. Expanding insect pollinators in the Anthropocene. Biological Reviews. Doi: 10.111/brv.12777 Erickson, E., Patch, H.M. and C.M. Grozinger. “Herbaceous perennial ornamental plants can support complex pollinator communities” Scientific Reports 11:17352 https://doi.org/10.1038/s41598-021-95892-w (2021). Lee, M.R., McNeil, D.J., Mathis, C.L., Grozinger, C.M., and J.L. Larkin, “Microhabitats created by log landings support abundant flowers and insect pollinators within regenerating mixed-oak stands in the Central Appalachian Mountains”.  Forest Ecology and Management 497: 119472 https://doi.org/10.1016/j.foreco.2021.119472 (2021). Mathis, C.L., McNeil, D.J., Lee, M.R., Grozinger, C.M., King, D.I., Otto, C.R.V., and J. L. Larkin. “Pollinator communities vary with vegetation structure and time since management within regenerating timber harvests of the Central Appalachian Mountains” Forest Ecology and Management 496: 119373 https://doi.org/10.1016/j.foreco.2021.119373 (2021). Crone, M.K. and C.M. Grozinger. “Pollen protein and lipid content influence resilience to insecticides in honey bees (Apis mellifera)”.  Journal of Experimental Biology 224 (9): jeb242040 https://doi.org/10.1242/jeb.242040 (2021). Alzaabi, O., Al-Khaldi, M.M., Ayotte, K., Pealoza, D., Urbina, J., Breakall, J.K., Lanagan, M., Patch, H.M., and C. M. Grozinger.  “Numerical Modeling and Measurement of Apis Mellifera Radar Scattering Properties” Geoscience and Remote Sensing Letters DOI: 10.1109/LGRS.2020.3048654 (2021). Jordan, A., Patch, H.M., Grozinger, C.M., and V. Khanna. “Economic Dependence and Vulnerability of United States Agricultural Sector on Insect-Mediated Pollination Service”  Environmental Science and Technology 55(4): 2243-2253 https://doi.org/10.1021/acs.est.0c04786 (2021). Kammerer, M., Goslee, S., Douglas, M.R., Tooker, J.F., Grozinger, C.M. “Wild bees as winners and losers: relative impacts of landscape composition, quality, and climate.” Global Change Biology January 12 <a href="https://doi.org/10.1111/gcb.15485%20(2021">https://doi.org/10.1111/gcb.15485 (2021</a> McAfee, A., D. R. Tarpy, and L. J. Foster. (2021). Queens exhibit variation in resilience to temperature stress. PLoS ONE, 16: e0255381. McAfee, A., J. P. Milone, B. N. Metz, E. McDermott, L. J. Foster, and D. R. Tarpy. (2021). Honey bee queen health is unaffected by contact exposure to pesticides commonly found in beeswax. Scientific Reports, 11: 15151. Milone, J. P. and D. R. Tarpy. (2021). Effects of developmental exposure to pesticides in wax and pollen on honey bee (Apis mellifera) queen reproductive phenotypes. Scientific Reports, 11: 1020. McAfee, A., A. Chapman, L. J. Foster, J. S. Pettis, and D. R. Tarpy. (2021). Trade-offs between sperm viability and immune protein expression in honey bee queens (Apis mellifera). Communication Biology, 4: 48. Milone, J. P.*, Chakrabarti, P.* , Sagili, R. and Tarpy, D.R.. (2021). Honey bee (Apis mellifera) royal jelly is qualitatively and quantitatively affected by colony level pesticide exposure. Chemosphere, 128183. Ricke DF, Lin C-H, Johnson RM. 2021. Pollen Treated with a Combination of Agrochemicals Commonly Applied During Almond Bloom Reduces the Emergence Rate and Longevity of Honey Bee (Hymenoptera: Apidae) Queens. J Insect Sci. 21(6). doi:10.1093/jisesa/ieab074 Walker EK, Brock GN, Arvidson RS, Johnson RM. 2022. Acute Toxicity of Fungicide-Insecticide-Adjuvant Combinations Applied to Almonds During Bloom on Adult Honey Bees. Environ Toxicol Chem. doi:10.1002/etc.5297. <a href="http://dx.doi.org/10.1002/etc.5297">http://dx.doi.org/10.1002/etc.5297</a>. Lin, C-H., Sponsler, D.B., Richardson, R.T., Watters, H.D., Glinski, D.A., Henderson, W.M., Johnson, R.M. 2020. Honey bees and neonicotinoid-treated corn seed: contamination, exposure, and effects. Environmental Toxicology and Chemistry 10.1002/etc.4957. Metz, B.N., Chakrabarti, P. and Sagili, R.R. (2021) Honey bee nursing responses to cuticular cues emanating from short-term changes in larval rearing environment. Journal of Insect Science 21: 7. Tsuruda, J.M.#, Chakrabarti, P.# and Sagili, R.R. (2021) Honey Bee Nutrition. Veterinary Clinics of North America: Food Animal Practice – Honey Bee Veterinary Medicine.  DOI: 10.1016/j.cvfa.2021.06.006. (# Equal first author contributions) Topitzhofer, E., Lucas, H.M., Carlson, E.A., Chakrabarti, P., Sagili, R.R. (2021) Collection and Identification of Pollen from Honey Bee Colonies. Journal of Visualized Experiments DOI: 10.3791/62064. Strobl, V., Bruckner, S., Radford, S., Wolf, S., Albrecht, M., Villamar-Bouza, L., Maitip, J., Kolari, E., Chantawannakul, P., Glauser, G., Williams, G.R., Neumann, P., Straub, L. 2021. No impact of neonicotinoids on male solitary bees Osmia cornuta under semi-field conditions. Physiological Entomology 46, 105-109. Tosi, S., Nieh, J.C, Brandt, A., Coll, M., Fourrier, J., Giffard, H., Hernández-López, J., Malagnini, V., Williams, G.R., Simon-Delso, N. 2021. Long-term field-realistic exposure to a next-generation pesticide, flupyradifurone, impairs honey bee behaviour and survival. Communications Biology 4, 805. Minnameyer, A., Strobl, V., *Bruckner, S., Van Oystaeyan, A., Wackers, F., Williams, G.R., Yañez, O., Neumann, P., Straub, L. 2021. Eusocial insect declines: insecticide impairs sperm and feeding glands in bumblebees. Science of The Total Environment 785, 146955. Carr-Markell MK, Demler CM, Couvillon 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. Carr-Markell MK, Spivak M. 2020. External validation of the new calibration for mapping honey bee waggle dances.  Animal Behaviour. <a href="https://doi.org/10.1016/j.anbehav.2020.12.006">https://doi.org/10.1016/j.anbehav.2020.12.006</a>. Drummond, Francis A., Jennifer Lund, and Brian Eitzer.2021. Honey Bee Health in Maine Wild Blueberry Production. Insects 12: 523. Krichilsky, E., Centrella, M., Eitzer, B., Danforth, B., Poveda, K. and Grab, H., 2021. Landscape composition and fungicide exposure influence host–pathogen dynamics in a solitary bee. Environmental Entomology, 50: 107-116. Démares, F.J., D. Schmehl, J.R. Bloomquist, A.R. Cabrera, Z.Y. Huang, P. Lau, J. Rangel, J. Sullivan, X. Xie, J.D. Ellis. 2021. Honey bee (Apis mellifera) exposure to pesticide residues in nectar and pollen in urban and suburban environments from four regions of the United States. Accepted. Urban-Mead, K., P. Muñiz, J. Gillung, A. Espinoza, R. Fordyce, M. Van Dyle, S.H McArt, and B.N. Danforth (2021). Bees in the trees: Diverse spring fauna in temperate forest edge canopies. Forest Ecology and Management 482 [published online 8 Jan, 2021:https://doi.org/10.1016/j.foreco.2020.118903] [entered] Senapathi, D. et al. (2021). Wild insect diversity increases inter-annual stability in global crop pollinator communities. Proceedings of the Royal Society of London B (Biological Sciences) 288: 20210212 [published online 17 March 2021; <a href="https://doi.org/10.1098/rspb.2021.0212">https://doi.org/10.1098/rspb.2021.0212</a>] [entered] Topitzhofer E, Hedstrom C, Chakrabarti P, Melathopoulos A, Rondon S, Langellotto G, Sagili R. 2020. Asian Giant Hornet: A potential threat to honeybee colonies in Oregon. OSU Extension Service EM 9297. Butters, J., B. J. Spiesman, and T. N. Kim. Fire rotation and bison presence have indirect below- and above-ground effects on specific pollinator communities; in review.   Objective 2: Genetics, Breeding, Diversity McGrady CM, Strange JP, López-Uribe MM, Fleischer SJ. (2021) Wild bumble bee colony abundance, scaled by field size, predicts pollination services. Ecosphere 12: e03735 López-Uribe MM. (2021). Wild Bees: Diversity, Ecology, and Stressors of Non-Apis Bees. Honey Bee Medicine for the Veterinary Practitioner, (eds T.R. Kane and C.M. Faux). Chapter 7: 81-91. https://doi.org/10.1002/9781119583417.ch7 Jones LJ, Kilpatrick SK, López-Uribe MM. (2021) Gynandromorph of the squash bee Eucera (Peponapis) pruinosa from an agricultural field in central Pennsylvania, United States of America. Journal of Melittology 100: 1-10 Galbraith, D.A., Ma, R. and C.M. Grozinger. “Tissue specific transcription patterns support the kinship theory of intragenomic conflict in honey bees (Apis mellifera)”  Molecular Ecology 30 (4), 1029-1041https://doi.org/10.1111/mec.15778 (2021). Dogantzis, K.A., Tiwari, T., Conflitti, I.A., Patch, H.M., Muli, E.M., Garnery, L., Whitfield, C.W., Stolle, E., Alqarni, A.S., Allsopp, M.H., and A. Zayed. ‘Thrice out of Asia and the adaptive radiation of the western honey bee.” Science Advances. 7(49) <a href="https://doi.org/10.1126/sciadv.abj2151">DOI: 10.1126/sciadv.abj2151</a> McCabe LM, Boyle NK, Scalici MB, Pitts-Singer TL. 2021. Adult body size measurement redundancies in Osmia lignaria and Megachile rotundata (Hymenoptera: Megachilidae) PeerJ 9:e12344 <a href="https://doi.org/10.7717/peerj.12344">https://doi.org/10.7717/peerj.12344</a> Slater G.P., Smith N.M.A., Harpur BA. (2021). Prospects in Connecting Genetic Variation to Variation in Fertility in Male Bees. Genes. DOI:10.3390/genes12081251. Kaskinova M., Yunusbayev B., Altinbaev R., Raffiudin R., Carpenter M.H., Nikolenko A, Harpur B.A. & Yunusbaev, U. (2021). Improved Apis mellifera reference genome based on the alternative long-read-based assemblies. G3. p. 2021.04.30.442202. DOI: 10.1093/g3journal/jkab223 Harpur B.A. & Rehan S.M. (2021). Connecting social polymorphism to single nucleotide polymorphism: population genomics of the small carpenter bee, Ceratina australensis. Biol J Linn Soc Lond., DOI: https://doi.org/10.1007/s13592-020-00836-4 doi:10.1093/biolinnean/blab003 Carpenter, M.H. & Harpur, B. A. (2021). Genetic Past, Present, and Future of the Honey Bee (Apis mellifera) in the United States. Apidologie. DOI: https://doi.org/10.1007/s13592-020-00836-4 [Invited Review; Featured in the American Bee Journal] Qin J, Liu F, Luo S, Wu J, He S, Imran M, Ye W, Lou W, Li-Byarlay H, The Molecular Characterization and Gene Expressions of Trehalase in Bumblebee, Bombus lantschouensis (Hymenoptera: Apidae). Sociobiology 68(4), e5443. Swami R, Ganser B, Strand M, Tarpy D, Li-Byarlay H@, Assessment and comparison of two different extraction methods on nucleic acids from individual honey bees, Annals of the Entomological Society of America, accepted (DOI: saab027). Smith J, Cleare X, Given K, Li-Byarlay H@, 2021. Morphological changes in the mandibles accompany the defensive behavior of Indiana mite biting honey bees against Varroa destructor, Frontiers in Ecology and Evolution doi: 10.3389/fevo.2021.638308 Metz, B. N. and D. R. Tarpy. (2021). Reproductive and morphological quality of commercial honey bee (Hymenoptera: Apidae) drones in the United States. Journal of Insect Science, 21: 2. Rusert, L. M., J. S. Pettis, and D. R. Tarpy. (2021). Introduction of Varroa destructor has not altered honey bee queen mating success in the Hawaiian archipelago. Scientific Reports, 11: 1366. 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. Liu, F. L. Wu, Y. Zhang, L. Li, Q. Li, Z.Y. Huang*, H. Zhao*. 2021. Mblk-1 regulates sugar responsiveness in honey bee (Apis mellifera) foragers.  Insect Science. <a href="https://doi.org/10.1111/1744-7917.12971">https://doi.org/10.1111/1744-7917.12971</a>   Objective 3: Management Evans KC, Underwood RM, López-Uribe MM. (2021) Combined effects of oxalic acid sublimation and brood breaks on Varroa Mite (Varroa destructor) and Deformed Wing Virus levels in newly established honey bee (Apis mellifera) colonies. Journal of Apicultural Research: 1-9. Robinson, A.C., Peeler, J.L., Prestby, T., Goslee, S.C., Anton, K., and C. M. Grozinger. Beescape: Characterizing User Needs for Environmental Decision Support in Beekeeping Ecological Informatics 64: 101366 https://doi.org/10.1016/j.ecoinf.2021.101366 (2021). Calovi, M., Grozinger. C., Miller, D., Goslee, S. Summer weather conditions influence winter survival of honey bees (Apis mellifera) in the northeastern United States. Scientific Reports 11: 1553 https://doi.org/10.1038/s41598-021-81051-8 (2021) Allen-Perkins, A., et al. and Bartomeus, I. (2022), CropPol: a dynamic, open and global database on crop pollination. Ecology e3614. <a href="https://doi.org/10.1002/ecy.3614">https://doi.org/10.1002/ecy.3614</a> Harpur, B.A. (2021) Indiana Solar Site Pollinator Habitat Planning Scorecard (POL-10-W) Harpur, B.A., & Ploessl, S.* (2021) What is Pollinator-Friendly Solar? (ID-522) Tarpy, D. R., E. Talley, and B. N. Metz. (2021). Influence of brood pheromone on honey bee colony establishment and queen replacement. Journal of Apicultural Research, 60: 220-228. Kulhanek, K., N. Steinhauer, J. Wilkes, M. Wilson, M. Spivak, R. Sagili, D. R. Tarpy, E. McDermott, A. Garavito, K. Rennich, and D. vanEngelsdorp. (2021). Survey-derived best beekeeping management practices improve colony health and reduce mortality. PLoS ONE, 16: e0245490. Potter, D.A.; Redmond, C.T.; McNamara, T.D.; Munshaw, G.C. Dwarf White Clover Supports Pollinators, Augments Nitrogen in Clover–Turfgrass Lawns, and Suppresses Root-Feeding Grubs in Monoculture but Not in Mixed Swards. Sustainability 2021, 13, 11801. https://doi.org/10.3390/su132111801 Hopkins, B.K., Chakrabarti, P., Lucas, H.M., Sagili, R.R. and Sheppard, W.S. (2021) Impacts of different winter storage conditions on the physiology of diutinus honey bees (Apis mellifera L.). Journal of Economic Entomology toaa302: 1-6. <a href="https://doi.org/10.1093/jee/toaa302">https://doi.org/10.1093/jee/toaa302</a>. Butters, J., Murrell, E., Spiesman, B. J., and T.N. Kim.  Environmental Entomology. Native flowering border crops attract high pollinator abundance and diversity, providing growers the opportunity to enhance pollination services; accepted. Sheppard, Walter S.   Honey Bee Pests. 2021.  In: Hollingsworth, C.S., editor. Pacific Northwest Insect Management Handbook. Corvallis, OR: Oregon State University. C8-C9. Hopkins, B.K., Chakrabarti , P., Lucas, H., Sagili, R., Sheppard W.S.  2021. Impacts of different winter storage conditions on the physiology of diutinus honey bees (Apis mellifera L.) J. Econ. Entomol. 114:409-414  <a href="https://urldefense.com/v3/__http:/dx.doi.org/10.1093/jee/toaa302__;!!JmPEgBY0HMszNaDT!7xu-iwXwTiG6ZiPoFGFix4RFI4XnbOdOMvNU-C0hlrA_VIWg_Y8xVTfkixdEslHg$">10.1093/jee/toaa302</a> Kulhanek, K., Hopkins, B.K. and Sheppard, W.S.  Comparison of Oxalic Acid Drip and HopGuard for pre-winter Varroa destructor control in honey bee (Apis mellifera) colonies. J. Apic. Res. Accepted - In Press   Other Publications Jones LJ, Ford RP, Schilder RJ, López-Uribe MM. (2021) Honey bee viruses are highly prevalent but at low intensities Chen X, Liu B, Li X, An TT, Zhou Y, Li G, Wu-Smart J, Alvarez S, Naldrett MJ, Eudy J, Kubik G, Wilson RA, Kachman SD, Cui J, Yu J. 2021. Identification of anti-inflammatory vesicle-like nanoparticles in honey. J Extracell Vesicles 10(4):e12069. doi: 10.1002/jev2.12069. Epub 2021 Feb 12. PMID: 33613874; PMCID: PMC7879699. Shanahan M, Spivak M. 2021. Resin use by stingless bees:  A review. Insects.  12, 719. https://doi.org/10.3390/insects12080719

Impact Statements

Auburn University (Williams) coordinated a virtual monthly beekeeping seminar series – At Home Beekeeping – alongside apicultural specialists and scientists from the eastern United States (Ellis & Jack, UF; Delaplane & Berry, Georgia; Tarpy, North Carolina State; Webster, Kentucky State; Tsuruda, Tennessee; Chakrabarti Basu, Mississippi State; Healy, Louisiana State; Simone-Finstrom & Lau, USDA-ARS; Rangel, TAMU. That program has been hugely popular, attended by over 2,300 participants during the reporting period. Overall, 89% and 69% of participants indicated that they plan to implement learned practices and that attendance will save them money moving forward, respectively.

Date of Annual Report: 03/01/2023

Report Information

Annual Meeting Dates: 01/05/2023 - 01/05/2023
Period the Report Covers: 01/01/2022 - 12/31/2022

Participants

Amiri, Esmaeil; Mississippi State University
Chakrabarti-Basu, Priyadarshini; Mississippi State University
Delaplane, Keith; University of Georgia
Ellis, James; University of Florida
Flenniken, Michelle; Montana State University
Harpur, Brock; Purdue University
Huang, Zachary; Michigan State University
Jack, Cameron; University of Florida
Johnson, Reed; Ohio State University
López-Uribe, Margarita; Pennsylvania State University
Rangel-Posada, Juliana; Texas AgriLife Research
Sagili, Ramesh; Oregon State University
Spivak, Marla; University of Minnesota
Tarpy, David; North Carolina State University
Williams, Geoffrey; Auburn University
Wu-Smart, Judy; University of Nebraska

Brief Summary of Minutes

Brief Summary of Annual NC1173 Multi-State Project Meeting

Minutes were taken by Margarita López-Uribe (Penn State)

The NC1173 business meeting was conducted as part of the 2023 American Bee Research Conference (ABRC) with the American Association of Professional Apiculturists (AAPA) meeting. We met in Jacksonville, FL on January 5 and 6 2023 during the American Beekeeping Federation (ABF) Meeting. The ABRC meeting serves as the scientific program for the NC1173 multi-state group. A detailed agenda for the ABRC meeting can be found online (https://aapa.cyberbee.net/2022/abrc-2023-final-agenda/), and it was submitted in conjunction with this report. The proceedings of the conference will be published in the coming months in bee Culture.

The business meeting was called to order at 5:00 pm EST by chairperson Dr. Margarita López-Uribe from Penn State University. The Project Director / Administrative Advisor, Dr. Brian McCornack (Kansas State University) joined the meeting via zoom. Of the 41 current members listed in NIMMS, 14 were in attendance during the meeting.

The first point was to review the current status of the multi-state project. Dr. Margarita López-Uribe reminded everyone of the objectives of the project and the timeline (10/01/2019 to 09/30/2024), and that we will need to submit a new project by the end of the year. The new timeline includes three steps: (1) Request to write a proposal (9/15); (2) Submit new project objectives (10/15); and (3) Submit the full new proposal to NIMSS. Members who have previously submitted renewal projects (including Drs. Reed Johnson, Judy Wu-Smart, Marla Spivak, and Juliana Rangel-Posada) and others, including Michelle Flenniken and David Tarpy, provided valuable input including the suggestion to use previous projects submitted and using the ABRC proceedings to guide the future directions of the NC1173 project.

Dr. Brian McCornack encouraged this group to work on better synthesizing the information in the report and try to highlight the collaborative multi-state efforts instead of focusing on the efforts of individual members of the group.

Members discussed that an important point to be considered for a new multi-state project is the incorporation of objectives that are more holistic including pollinator health beyond honey bees.

The NC1173 project renewal team includes Dr. Margarita López-Uribe (Chair in 2023), Dr. Priyadarshini Chakrabarti Basu (Vice-Chair in 2023) with assistance from Dr. Michelle Flenniken (previous Chair) and Dr. Judy Wu-Smart (previous Chair). Bryan Danforth and Rachel Winfree have expressed an interest in participating in the write-up of the new multi-state project to incorporate research objectives that are more relevant to other bees as well.

Dr. López-Uribe reminded all members that reports of all 2022 activities are due on January 27 2023 to be included in the NC1173 annual report on February 15th 2023.

Dr. McCornack suggested that we survey the NC1173 members that do not participate in the ABRC meeting and asked them what changes could be incorporated to increase their participation in the meeting and multi-state efforts.

Next year, we will meet with the American Beekeeping Federation (ABF) in New Orleans (LA) on January 11 and 12th 2024. Meeting was adjourned at 5:50 pm (EST).

Accomplishments

NC1173 Accomplishments:     Objective 1a: (Biotic Stressors: Pests & Pathogens) Honey bees are attacked by a large number of parasites and pathogens. Varroa destructor—an ectoparasitic mite that feeds on honey bees—is one of the deadliest pests currently facing the US beekeeping industry. Varroa mites transmit viruses within and between colonies, including deformed wing virus (DWV), which are often associated with overwinter losses of honey bee colonies. In addition, managed honey bees are threatened by bacterial (e.g., American and European Foulbrood) and eukaryotic pathogens (e.g., Vairimorpha) and other pests (e.g., small hive beetles). Growing evidence has demonstrated that some of these honey bee pathogens can be picked up by wild bees visiting shared floral resources with honey bees. This potential for pathogen transmission has raised concerns about the consequences that poor pest and disease management in honey bees may have on wild bee fauna.   Short-term Outcomes:   <ul> <li style="font-weight: 400;">Nothing to report</li> </ul> Outputs: <ul> <li style="font-weight: 400;">Development of new compounds against Varroa and tests for toxicity to adult honey bees in an effort to identify new active ingredients that might be useful in the fight against Varroa (Ellis and Jack, UF; Shepard, WSU; Johnson, OSU). Other developments include new assays investigating how behavioral responses linked to hygienic behavior may impact intra-colony virus transmission and Varroa control (Spivak, UM; Li-Byarlay Central State; and Rangel, TAMU).</li> <li style="font-weight: 400;">Studies on the mating biology and chemical ecology of small hive beetles are under development with the goal of better understanding what is driving their spread and establishment in new areas (Williams, Auburn). Assays for new compounds for small hive beetle control (including acetamiprid and fipronil) are under development (Jack and Ellis, UF).</li> <li style="font-weight: 400;">The efficacy of Oxytetracycline (OTC) is currently being tested to control European Foulbrood (EFB) disease in honey bee colonies pollinating early-season specialty crops such as blueberries (Sagili, OSU).</li> <li style="font-weight: 400;">Novel data directly linking virus levels in mites and bees are providing empirical support for the amplification of viruses using mites as vectors (Tarpy, NCSU). In addition, experimental work has demonstrated that Varroa mites favor different variants of Deformed Wing Virus (DWV) (Grozinger, PSU).</li> <li style="font-weight: 400;">Empirical studies surveying bees in North Carolina and Pennsylvania found no support for spillover of honey bee pathogens to wild bees (Tarpy, NCSU; López-Uribe, PSU). </li> <li style="font-weight: 400;">Studies incorporating landscape information with disease prevalence in bumble bees indicate that higher floral availability promotes healthier bees (Hines and Grozinger; PSU).</li> </ul> Activities: <ul> <li style="font-weight: 400;">Nothing to report.</li> </ul> Milestones: <ul> <li style="font-weight: 400;">Publish shared protocols for pathogen quantification in honey bees and wild bees to increase opportunities for meta-analyses of data collected across the United States.</li> </ul> Objective 1b: (Abiotic Stressors: Pesticides, Forage Availability, Nutrition) Major abiotic stressors contributing to honey bee health decline include pesticide exposure, malnutrition, and climatic instability. NC1173 members are assessing the effects of these interacting factors on bees and their pollination services through laboratory assays, field experiments and landscape-level data.  Short-term Outcomes:   <ul> <li style="font-weight: 400;">Published a pipeline for generating pesticide toxicity data at landscape scales across the United States (Grozinger, PSU). </li> </ul> Outputs: <ul> <li style="font-weight: 400;">The antagonistic interactions between malnutrition and insecticides negatively impacts traits linked to fitness and immunity traits such as sperm quality and hypopharyngeal gland activity (Williams, Auburn).</li> <li style="font-weight: 400;">Larval nutritional stress in bees can have long-lasting effects on honey bee health including their ability to respond to viral infection as adults (Walton, Dolezal, and Toth, ISU). Studies looking at the influence of nutrition (specifically phytosterols, protein and lipid ratios) on the outcome of pathogenic infections continued to be an active research are in several NC1173 labs (i.e., Sagili OSU; Rangel, TAMU; Grozinger, PSU).</li> <li style="font-weight: 400;">Models based on national weather data demonstrated that weather instability and extreme weather events are key drivers of honey bee colony losses in the United States (Williams, Auburn; Grozinger, PSU). </li> <li style="font-weight: 400;">A multi-institution team from PSU, MSU, USGS, WI demonstrated that poor weather conditions could be buffered by increasing the amount of herbaceous grassy land (Grozinger, PSU). Similar findings in soybean plantations highlight the benefits of natural prairie floral resources for bee health (Toth, ISU).</li> <li style="font-weight: 400;">Pesticide residue analyses on pollen from agricultural and urban sites indicate that pesticide exposure is lower in urban than in agricultural areas (Ellis, UF; Huang, MSU; Rangel, TAMU).</li> <li style="font-weight: 400;">Efforts related to toxicology have expanded to investigate the impact of fungicides and adjuvants on bee health. Preliminary analyses investigating the impact of fungicides on the development of solitary bees have no significant effects (Danforth, Cornell). In contrast, research on commonly used spray adjuvants has demonstrated greater toxicity to adult honey bees than the fungicides or insecticides that they are mixed with (Reed, OSU).</li> <li style="font-weight: 400;">A novel route of pesticide exposure to bees and wildlife was identified through the improper disposal of pesticide-treated expired seeds through ethanol production. This novel practice began in 2015 and has resulted in large, unprecedented amounts of waste laden with systemic pesticides, like neonicotinoids, leaching into the environment for years. These events have led to the development of a One Health framework to protect bees, wildlife, and humans from these types of toxic waste using a “systems approach” (Wu-Smart, UNL).</li> </ul> Activities: <ul> <li style="font-weight: 400;">Organized a pollen-collection training session at USGS Eastern Ecological Science Center, Laurel, MD (Sagili OSU). </li> <li style="font-weight: 400;">In 2022, a One Health internship was offered to students from different fields (pre-veterinary, fisheries and wildlife, and entomology majors) (Wu-Smart, UNL).</li> <li style="font-weight: 400;">At Home Beekeeping Webinar Series was attended by over 2,500 participants during the reporting period. Overall, 88% and 59% of participants indicated that they plan to implement learned practices and that attendance will save them money moving forward, respectively. (Ellis and Jack, UF; Delaplane and Berry, UGA; Tarpy, NCSU; Webster, KYS; Tsuruda, UTN; Chakrabarti Basu, MSU; Healy, LSU; Simone-Finstrom and Lau, USDA-ARS; Rangel, TAMU; Williams, Auburn)</li> </ul> Milestones: <ul> <li style="font-weight: 400;">Development of a pollen lipids, proteins, phytosterols and amino acids database that will be publicly available for researchers, policymakers, citizens, and stakeholders. </li> </ul>   Objective 2: (Genetics, Breeding, & Diversity) Breeding mite and disease resistant traits in honey bee stock and diversifying honey bee genetics and selection efforts are more sustainable solutions to address the pest and pathogen issues in honey bees and is a long-term goal for NC1173 members.  Short-term Outcomes:  Nothing to report  Outputs: <ul> <li style="font-weight: 400;">Novel developments on the implementation of genomic selection into breeding decisions with international collaborations (Harpur, Purdue) </li> <li style="font-weight: 400;">Studies of genetic diversity of honey bees in the United States are offering new insights into baseline levels of genetic diversity and levels of Africanization of populations in northern states (Harpur, Purdue; López-Uribe, PSU).</li> <li style="font-weight: 400;">Efforts to select for stocks with high grooming and mite biting behavior from local feral colonies (Li-Byarlay CSU; Harpur, Purdue). </li> <li style="font-weight: 400;">Side-by-side comparisons of honey bee stock performance indicate that locally bred stocks outperform other stocks in northern states (Harpur, Purdue; López-Uribe, PSU).</li> <li style="font-weight: 400;">Comparisons of virus levels (DWV) in feral and managed honey bees indicate that colonies show comparable levels of viruses in Texas (Rangel, TAMU). However, DWV strains from managed colonies are more virulent than the strains from feral colonies (Grozinger, PSU).</li> </ul> Activities: <ul> <li>Offered online programs (webinars) and field days to beekeepers on queen-rearing and grafting (Li-Byarlay CSU)</li> </ul> Milestones: <ul> <li style="font-weight: 400;">Joint review publication on the available honey bee stock in the United States and their phenotypic traits.</li> </ul>   Objective 3: (Management) Management practices to maintain healthy honey bees and landscapes that support pollinators are in high demand and recommendations continue to evolve with new research. Therefore, NC1173 members strive to engage in research activities that are relevant to stakeholder needs to better provide the most up-to-date, science-based recommendations to beekeepers, pesticide applicators, farmers, homeowners, and policymakers. Efforts for this objective include recommendations on how to better manage pests and pathogens in honey bees, enhancing landscapes for pollinators, and options to reduce exposure or mitigate the effects of pesticides.   Short-term Outcomes:   <ul> <li style="font-weight: 400;">Support for the practical implementation of rough box hives to support propolis collection and colony health (Spivak, UMN).</li> <li style="font-weight: 400;">Developed a rapid assessment protocol for ranking pollinator-attractive plants (Grozinger and Patch, PSU).</li> <li style="font-weight: 400;">Cooperation with a private company (Dalan Animal Health, LLC) for the development of a vaccine for American Foulbrood (AFB) (Delaplane, UGA).</li> </ul> Outputs: <ul> <li>Development of protocols and recommendations on how to integrate Varroa mite management using organic acids and cultural measures (López-Uribe, PSU; Williams, Auburn).</li> <li>New results on the implementation of thyme oil and thymol for immune stimulation of honey bees in response to virus infections (Flenniken, MSU).</li> </ul> <ul> <li style="font-weight: 400;">Successful implementation of the use of rough surface texture of hive boxes to enhance propolis collection in honey bees, which had positive impacts on colony population size and colony homeostasis (Spivak, UMN).</li> <li style="font-weight: 400;">Development and implementation of novel technologies for queen presence in honey bee colonies (via sound detections) (Huang, MSU).</li> <li style="font-weight: 400;">Analyses are underway to determine particular tree species are associated with diverse and abundant pollinator communities, and/or whether particular tree and bee species are associated. This information can be directly used for restoration efforts of pollination populations (Winfree, Rutgers).</li> <li style="font-weight: 400;">Data from pollination experiments of several crops across the United States indicate that there is pollinator limitation in about 25%-30% of crop fields (Winfree, Rutgers).</li> </ul> Activities: <ul> <li>Surveys indicate overwhelming enthusiasm for pollinator-friendly practices but gaps in knowledge about which practices are most effective and what tools are available to implement them. These results give general guidelines for the development of pollinator extension programs to address these knowledge gaps (Toth, ISU).</li> </ul> Milestones: <ul> <li style="font-weight: 400;">Centralized repository with documents about best management practices for honey bees and landscapes for different regions across the United States.</li> </ul>

Publications

NC1173 Member Publications (01/01/2022 to 12/31/2022) *Papers applicable to multiple objectives are only reported once.   Summary table and list of publications by topic reported by NC1173 committee members for 2020. NC1173 authors are indicated in bold. <table> <tbody> <tr> <td> Publications by topic </td> <td> 2022 </td> </tr> <tr> <td> Obj 1a: Biotic (Pests & pathogens) </td> <td> 8 </td> </tr> <tr> <td> Obj 1b: Abiotic (Pesticides, nutrition, landscapes)  </td> <td> 35 </td> </tr> <tr> <td> Obj 2: Genetics, Breeding, Diversity </td> <td> 1 </td> </tr> <tr> <td> Obj 3: Management </td> <td> 10 </td> </tr> <tr> <td> Other Publications </td> <td> 10 </td> </tr> <tr> <td> Total </td> <td> 64 </td> </tr> <tr> <td> Publications with >1 NC1173 authors </td> <td> 13 </td> </tr> </tbody> </table>   Objective 1a: Biotic Stressors (Pests & pathogens) Bartlett, L.J., Martinez-Mejia, C., Delaplane, K.S. 2022. Honey bees (Apis mellifera Hymenoptera: Apidae) preferentially avoid sugar solutions supplemented with field-relevant concentrations of hydrogen peroxide despite high tolerance limits. J. Insect Sci. <a href="https://doi.org/10.1093/jisesa/ieab102">https://doi.org/10.1093/jisesa/ieab102</a> Chapman, A., E. Amiri, B. Han, E. McDermott, O. Rueppell, D. R. Tarpy, L. J. Foster, and A. McAfee. (2022). Cryptic costs of viral infection in a model social insect. Scientific Reports, 12: 15857. Cleary, D., Szalanski, A. L. 2022. Molecular Diagnostic Survey of Honey Bee, Apis mellifera L., Pathogens and Parasites from Arkansas, USA. Journal of Apicultural Science, 66(2), 149-158. 10.2478/JAS-2022-0014  Jones LJ, Singh A, Schilder RJ, López-Uribe MM. (2022) High parasite prevalence in the squash bees Eucera (Peponapis) pruinosa from the northeastern United States. Journal of Invertebrate Pathology 195: 107848. Levenson, H. K. and D. R. Tarpy. (2022). Effects of planted pollinator habitat on pathogen prevalence and interspecific detection between bee species. Scientific Reports, 12: 7806. Papach, A., Beaurepaire, A., Yañez, O., Huwiler, M., Williams, G.R., Neumann, P. 2022. Multiple mating by both sexes in an invasive insect species, Aethina tumida (Coleoptera: Nitidulidae). Insect Science<a href="https://doi.org/10.1111/1744-7917.13112"> https://doi.org/10.1111/1744-7917.13112</a> Papach, A., Balusu, R., Williams, G.R., Fadamiro, H.Y., Neumann, P. 2022. The smell of sex: cuticular hydrocarbons of adult small hive beetles, Aethina tumida (Coleoptera: Nitidulidae). Journal of Apicultural Research 61, 365-367. Walton, A., Toth A. L., Dolezal, A.G. 2021. Developmental environment shapes honeybee worker response to virus infection. Scientific reports 11 (1), 1-12   Objective 1b: Abiotic Stressors (Pesticides, nutrition, landscapes) Bartlett, L.J., Bruckner, S., Delaney, D.A., Williams, G.R., Delaplane, K.S., 2022. A computational approach to tracking age-based task frequency distributions of Apis mellifera worker cohorts. Journal of Apicultural Research, 61, 147-150. Carlson, E.A, Melathopoulos A and Sagili R (2022) The Value of Hazard Quotients in Honey Bee (Apis mellifera) Ecotoxicology: A Review. Front. Ecol. Evol. 10:824992. doi: 10.3389/fevo.2022.824992  Chakrabarti, P.# , Milone, J.P.^#, Sagili, R.R. and Tarpy, D.R. (2021) Colony-level pesticide exposure affects honey bee (Apis mellifera L.) royal jelly production and nutritional composition. Chemosphere 263: 128183. (# Equal first author contributions) Chakrabarti, P. and Sagili, R.R. (2020) Changes in honey bee head proteome in response to dietary 24-methylenecholesterol manipulation. Insects 11: 743. Chakrabarti, P., Carlson, E.A.^, Lucas, H.M., Melathopoulos, A. and Sagili, R.R. (2020) Field rates of Sivanto™ (flupyradifurone) and Transform® (sulfoxaflor) increase oxidative stress and induce apoptosis in honey bees (Apis mellifera L.). PLOS ONE 15(5): e0233033. Chakrabarti, P., Lucas, H.M. and Sagili, R.R. (2020) Novel Insights into Dietary Phytosterol Utilization and Its Fate in Honey Bees (Apis mellifera L.). Molecules 25: 571. Crone, M. K., Biddinger, D. J., and C.M. Grozinger. “Wild bee nutritional ecology: Integrative strategies to assess foraging preferences and nutritional requirements” Frontiers in Sustainable Food Systems 6:847003. doi: 10.3389/fsufs.2022.847003 Dai, W., Yang, Y., Patch, H.M., Grozinger, C.M., and J. Mu “Soil moisture affects plant-pollinator interactions in an annual flowering plant”  Philosophical Transactions B 3772021042320210423 <a href="http://doi.org/10.1098/rstb.2021.0423">http://doi.org/10.1098/rstb.2021.0423</a> Démares, F.J., Schmehl, D.R., Bloomquist, J.R., Cabrera, A.R., Huang, Z.Y., Lau, P., Rangel, J., Sullivan, J., Xie, X., Ellis, J.D. 2022. Honey bee (Apis mellifera) exposure to pesticide residues in nectar and pollen in urban and suburban environments from four regions of the United States. Environmental Toxicology and Chemistry, 41(4): 991-1003. https://doi.org/10.1002/etc.5298.  Douglas, M.R., Baisley, P., Soba, S., Kammerer, M.A., Lonsdorf, E.V., and C.M. Grozinger.  “Putting pesticides on the map for pollinator research and conservation” Scientific Data 9, 571  <a href="https://doi.org/10.1038/s41597-022-01584-z">https://doi.org/10.1038/s41597-022-01584-z</a> Erickson, E., Grozinger, C.M., and H.M. Patch. “Measuring plant attractiveness to pollinators: methods and considerations”  Journal of Environmental Entomology toac066, <a href="https://doi.org/10.1093/jee/toac066">https://doi.org/10.1093/jee/toac066</a> Frizzera, D., Ray, A., Seffin, E., Zanni, V., Annoscia, D., Grozinger, C. and F. Nazzi. “The beneficial effect of pollen on Varroa infected bees depends on its effects on behavioral maturation genes”  Frontiers in Insect Science  vol 2, <a href="https://doi.org/10.3389/finsc.2022.864238">https://doi.org/10.3389/finsc.2022.864238</a> Gupta Vakil, S.*, Biswas, S., Snow, D., Wu-Smart, J. 2022. Targeted Method for Quantifying Air-Borne Pesticide Residues from Conventional Seed Coat Treatments to Better Assess Exposure Risk During Maize Planting. Bull Environ Contam Toxicol 109, 1051–1058. <a href="https://doi.org/10.1007/s00128-022-03627-y">https://doi.org/10.1007/s00128-022-03627-y</a> Harvey J, Tougeron K, Gols R, Heinen R, Abarca M, Abram PK, Basset Y, Berg M, Boggs C, Brodeur J, Cardoso P, de Boer JG, De Snoo G, Deacon C, Dell JE, Desneux N, Dillon M, Duffy GA, Dyer L, Jacintha E, Espíndola A, Fordyce J, Forister M, Fukushima C, García-Robledo C, Gely C, Gobbi M, Hallmann C, Hance T, Harte J, Hochkirch A, Hof C, Kingsolver J, Lamarre GPA, Laurance W, Lavandero B, Le Lann C, Ma C-S; Ma G, Moiroux J, Monticelli L, Shah AA, Thakur MP, Thomas M, Van de Pol M, Verberk WCEP, Lehmann P, López-Uribe MM; Nice C, Ode P, Pincebourde S, Ripple W, Rowe M, Samways M, Sentis A, Stork N, Terblanche J, Tylianakis J, van Baaren J, van der Putten W, Wagner D, Van Dyck H, Chown S, Wyckhuys K, Woods HA, Wetzel W, Weisser W. (2022) Scientists’ warning on climate change and insects. Ecological Monographs e1553 <a href="https://doi.org/10.1002/ecm.1553">https://doi.org/10.1002/ecm.1553</a> Kumar, D., Banerjee, D., Chakrabarti, P., Sarkar, S. and Basu, P. (2022) Oxidative stress and apoptosis in Asian honey bees (A. cerana) exposed to multiple pesticides in intensive agricultural landscape. Apidologie 53: 25. Hall, M.J., Zhang, G., O’Neal, M.E., Bradbury, S.P. and Coats, J.R., 2022. Quantifying neonicotinoid insecticide residues in milkweed and other forbs sampled from prairie strips established in maize and soybean fields. Agriculture, Ecosystems & Environment, 325, p.107723. Heller, S.; Fine, J.; Phan, N.T.; Rajotte, E.G.; Biddinger, D.J.; Joshi, N.K. Toxicity of Formulated Systemic Insecticides Used in Apple Orchard Pest Management Programs to the Honey Bee (Apis mellifera (L.)). Environments 2022, 9, 90. <a href="https://doi.org/10.3390/environments9070090">https://doi.org/10.3390/environments9070090</a> Incorvaia, D.C., T. Dalrymple, Z.Y. Huang, F.C. Dyer. 2022. Short and long-term modulation of forager motivation by colony state in bumblebees. Animal Behavior,. 190: 61-70. <a href="https://doi.org/10.1016/j.anbehav.2022.05.007">https://doi.org/10.1016/j.anbehav.2022.05.007</a> Insolia, L., Molinari, R., Rogers, S.R., Williams, G.R., Chiaromonte, F., Calovi, M., 2022. Honey bee colony loss linked to parasites, pesticides and extreme weather across the United States. Scientific Reports 12, 20787. Levenson, H. K., A. Sharp, and D. R. Tarpy. (2022). Evaluating the impact of increased pollinator habitat in surrounding agricultural systems. Agriculture, Ecosystems, and Environment, 331: 107901. Lin C-H, Suresh S, Matcham E, Monagan P, Curtis H, Richardson RT, et al. Soybean is a Common Nectar Source for Honey Bees (Hymenoptera: Apidae) in a Midwestern Agricultural Landscape. J Econ Entomol. 2022;115: 1846–1851. doi:10.1093/jee/toac140 Mathis, C.L., Neil, D.J., Lee, M.R., Grozinger, C.M., Otto, C.R.V., and J. L. Larkin. “ Can’t See the Flowers for the Trees: Factors Driving Floral Abundance within Early-successional Forests in the Central Appalachian Mountains” Canadian Journal of Forest Research <a href="https://doi.org/10.1139/cjfr-2022-0014">https://doi.org/10.1139/cjfr-2022-0014</a> McAfee, A., B. N. Metz, J. P. Milone, L. J. Foster, and D. R. Tarpy. (2022). Drone honey bees (Apis mellifera) are disproportionately sensitive to abiotic stressors despite expressing high levels of stress response proteins. Communication Biology, 5: 141. McMinn-Sauder H, Lin C-H, Eaton T, Johnson R. A comparison of springtime pollen and nectar foraging in honey bees kept in urban and agricultural environments. Front Sustain Food Syst. 2022;6. doi:10.3389/fsufs.2022.825137 McLaughlin, R., Keller, J., Wagner, E., Biddinger, D., Grozinger, C. and K. Hoover.  “Insect visitors of black cherry (Prunus serotina) (Rosales: Rosaceae) and factors affecting viable seed production” Environmental Entomology nvab141, <a href="https://doi.org/10.1093/ee/nvab14">https://doi.org/10.1093/ee/nvab14</a> Metz, B.N., Chakrabarti, P. and Sagili R.R. (2021) Honey bee nursing responses to cuticular cues emanating from short-term changes in larval rearing environment. Journal of Insect Science 21: 7. Overturf, K.A., Steinhauer, N., Molinari, R., Wilson, M.E., Watt, A.C., Cross, R.M., vanEngelsdorp, D., Williams, G.R., Rogers, S.R. 2022. Winter weather predicts honey bee colony loss at the national scale. Ecological Indicators 145, 109709. Prestby, T.J., Robinson, A.C., McLaughlin, D., Dudas, P.M., and C.M. Grozinger. “Characterizing user needs for Beescape: A spatial decision support tool focused on pollinator health”  Journal of Environmental Management 325: 116416 (2023).  <a href="https://doi.org/10.1016/j.jenvman.2022.116416">https://doi.org/10.1016/j.jenvman.2022.1164</a> Price, B.E , Breece C, Galindo G, Greenhalgh A, Sagili R, Choi M, Lee J (2022) Nonnutritive Sugars for Spotted-Wing Drosophila (Diptera: Drosophilidae) Control Have Minimal Nontarget Effects on Honey Bee Larvae, a Pupal Parasitoid, and Yellow Jackets, Environmental Entomology, nvac095, <a href="https://doi.org/10.1093/ee/nvac095">https://doi.org/10.1093/ee/nvac095</a> Quinlan GM, Sponsler D, Gaines-Day HR, McMinn-Sauder HBG, Otto CRV, Smart AH, Colin T, Gratton C, Isaacs R, Johnson R, Milbrath MO, Grozinger CM. Grassy–herbaceous land moderates regional climate effects on honey bee colonies in the Northcentral US. Environ Res Lett. 2022;17: 064036. doi:10.1088/1748-9326/ac7063 Straub, L., Strobl, V., Bruckner, S., Camenzind, D.W., Van Oystaeyen, A., Wäckers, F., Williams, G.R., Neumann, P. 2022. Buffered fitness components: Antagonism between malnutrition and an insecticide in bumble bees. Science of The Total Environment 833, 155098. Topitzhofer, E., Lucas, H.M., Carlson, E.A.^, Chakrabarti, P., Sagili, R.R. (2021) Collection and Identification of Pollen from Honey Bee Colonies. Journal of Visualized Experiments. DOI: 10.3791/62064. Tsuruda, J.M.#, Chakrabarti, P.# and Sagili, R.R. (2021) Honey Bee Nutrition. Veterinary Clinics of North America: Food Animal Practice – Honey Bee Veterinary Medicine. Invited review currently in press. (# Equal first author contributions) Walker EK, Brock GN, Arvidson RS, Johnson RM. Acute toxicity of fungicide-insecticide-adjuvant combinations applied to almonds during bloom on adult honey bees. Environ Toxicol Chem. 2022;41: 1042–1053. doi:10.1002/etc.5297 Zhang, G., St. Clair, A.L., Dolezal, A.G., Toth, A.L. and O’Neal, M.E., 2022. Can native plants mitigate climate-related forage dearth for honey bees (Hymenoptera: Apidae)?. Journal of economic entomology, 115(1), pp.1-9.   Objective 2: Genetics, Breeding, Diversity Metz, B. N. and D. R. Tarpy. (2022). Variation in drone size leads to different life history decisions consistent with varying, long-term mating strategy. PeerJ, 10: e13859.   Objective 3: Management Berry, J., Bartlett, L.J., Bruckner, S., Baker, C., Braman, K., Delaplane, K.S., Williams, G.R. 2022. Assessing repeated oxalic acid vaporization in honey bee (Apis mellifera) colonies for control of the ectoparasitic mite Varroa destructor. Journal of Insect Science 22,<a href="https://doi.org/10.1093/jisesa/ieab089"> https://doi.org/10.1093/jisesa/ieab089</a>. Borchardt, K.E., Morales, C.L., Aizen, M.A. and Toth, A.L., 2021. Plant–pollinator conservation from the perspective of systems-ecology. Current Opinion in Insect Science, 47, pp.154-161. Cass, R.P., Hodgson, E.W., O’Neal, M.E., Toth, A.L. and Dolezal, A.G., 2022. Attitudes About Honey Bees and Pollinator-Friendly Practices: A Survey of Iowan Beekeepers, Farmers, and Landowners. Journal of Integrated Pest Management, 13(1), p.30. Dolezal, A.G., Torres, J. and O’Neal, M.E., 2021. Can solar energy fuel pollinator conservation?. Environmental entomology, 50(4), pp.757-761. Hopkins, B.K., Chakrabarti, P., Lucas, H.M., Sagili, R.R. and Sheppard, W.S. (2021) Impacts of different winter storage conditions on the physiology of diutinus honey bees (Apis mellifera L.). Journal of Economic Entomology toaa302: 1-6. Jack, C.J., Kleckner, K., Demares, F., Rault, L.C., Anderson, T.D., Carlier, P.R., Bloomquist, J.R., Ellis, J.D. 2022. Testing new compounds for efficacy against Varroa destructor and safety to honey bees (Apis mellifera). Pest Management Science, 78: 159-165. <a href="https://doi.org/10.1002/ps.6617">https://doi.org/10.1002/ps.6617</a>. Kleckner, K., De Carolis, A., Jack, C., Stuhl, C., Formato, G., Ellis, J.D. 2022. A novel acute toxicity bioassay and field trial to evaluate compounds for small hive beetle control. Applied Sciences, 12, 9905. <a href="https://doi.org/10.3390/app12199905">https://doi.org/10.3390/app12199905</a>.  Kline, O.; Phan, N.T.; Porras, M.F.; Chavana, J.; Little, C.Z.; Stemet, L.; Acharya, R.S.; Biddinger, D.J.; Reddy, G.V.P.; Rajotte, E.G.; Joshi, N.K. Biology, Genetic Diversity, and Conservation of Wild Bees in Tree Fruit Orchards. Biology 2023, 12, 31. <a href="https://doi.org/10.3390/biology12010031">https://doi.org/10.3390/biology12010031</a> Lamke, K., Wedin D., and Wu-Smart, J. 2022. Remnant prairies and high-diversity restorations support wild bees season-long. The Prairie Naturalist Journal Special Edition 1: 30-40.  Simone-Finstrom, M., M. K. Strand, D. R. Tarpy, and O. Rueppell. (2022). Impact of honey bee migratory management on pathogen loads and immune gene expression is affected by complex interactions with environment, worker life history, and season. Journal of Insect Science, 22: 17: 1–10.   Other publications Aldercotte A, D T Simpson, and R Winfree. 2022. Crop visitation by wild bees declines over an eight-year time series —a dramatic trend, or just dramatic between-year variation? Insect Conservation and Diversity. DOI: 10.1111/icad.12589  Andrade TO, Ramos KS, López-Uribe MM, Branstetter MG, Brandão CRF. (2022) Integrative approach resolves the taxonomy of Eulaema cingulata (Apidae, Euglossini), an important pollinator in the Neotropics. Journal of Hymenoptera Research 94: 247–269 Dharampal, P., B.N. Danforth, S. Steffan (2022). Exosymbiotic microbes within fermented pollen-provisions are as important for the development of solitary bees as the pollen, itself. Ecology and Evolution 2022;12:e8788 [published online 7 April, 2022; <a href="https://doi.org/10.1002/ece3.8788">https://doi.org/10.1002/ece3.8788</a>] Genung, M A, Reilly, N M Williams, A Buderi, J Gardner, and R Winfree. 2023. Rare and declining bee species are key to consistent pollination of wildflowers and crops across large spatial scales. Ecology  104: e3899   https://doi.org/10.1002/ecy.3899 Han, B., Q. Wei, E. Amiri, H. Hu, L. Meng, M. K. Strand, D. R. Tarpy, S. Xu, and O. Rueppell. (2022). The molecular basis of socially induced egg size plasticity in honey bees. eLife, 11: e80499. Hines HM, Kilpatrick SK, Mikó I, Snellings D, López-Uribe MM, Tian L. (2022) The diversity, evolution, and development of setal morphologies in bumble bees (Hymenoptera: Apidae: Bombus spp.). PeerJ 10: e14555 Lemanski, N, N M Williams, and R Winfree. 2022. Greater bee diversity is needed to maintain crop pollination over time. Nature Ecology and Evolution https://doi.org/10.1038/s41559-022-01847-3  Simpson, D T, L R Weinman, M A Genung, M E Roswell, M MacLeod, and R Winfree. 2022. Many bee species, including rare species, are important for function of entire plant-pollinator networks. Proceedings of the Royal Society of London, Series B 289: 20212689 https://doi.org/10.1098/rspb.2021.2689  Smith, C,  Harrison, J Gardner, and R Winfree. 2021. Forest-associated bees persist amid forest loss and regrowth in eastern North America.  Biological Conservation 260: 109202 <a href="https://doi.org/10.1016/j.biocon.2021.109202">https://doi.org/10.1016/j.biocon.2021.109202</a> Turley NE&upsih;, Biddinger DJ, Joshi NK, López-Uribe MM. (2022) Six years of wild bee monitoring shows changes in biodiversity within and across years and declines in abundance. Ecology and Evolution: 12(8):e9190  Wu X, Bhatia N, Grozinger CM, Yi SV. Comparative studies of genomic and epigenetic factors influencing transcriptional variation in two insect species. G3 (Bethesda) 12(11):jkac230. doi: 10.1093/g3journal/jkac230

Impact Statements

Supporting healthier managed and wild pollinators is critical for ecosystem function and sustainable agriculture. To help advance our knowledge and develop potential strategies to mitigate the multiple stressors that pollinator populations face, members of the NC1173 research group have made significant progress in gaining a fundamental understanding of the impact of biotic and abiotic stressors and their interactions on pollinator health. Efforts on fundamental and applied research have allowed for the incorporation of breeding and management tools to help mitigate the negative impacts of these stressors. Knowledge about these research advances has been transferred to thousands of beekeepers, farmers, and landowners this past year. Changes in land management practices that offer better nutrition and safer pesticide application methods have helped mitigate other stressors, such as climate and pathogens pressure. Overall, the research and education programs led by this team are providing critical information to improve managed and wild pollinator health across the U.S.

Date of Annual Report: 02/28/2023

Report Information

Annual Meeting Dates: 01/11/2024 - 01/11/2024
Period the Report Covers: 01/01/2023 - 12/31/2023

Participants

List of attendees in person:
Priya Chakrabarti Basu
Margarita López-Uribe
Judy Wu-Smart
Kate Anton (for Christina Grozinger)
Ana Heck
Robyn Underwood
Jamie Ellis
Declan Schroeder
David Wick
Cameron Jack
Lewis Bartlett
Brock Harpur
Juliana Rangel
David R. Tarpy
Zachary Huang
Reed Johnson
Esmaeil Amiri
Hongmei Li-Byarlay
Michelle Flenniken

List of attendees via Zoom:
Christine Hamilton
Jeffrey Harris
Brian Spiesman
Geoffrey Williams
Rachel Vannette
Hollis Woodard
Tania Kim
Ramesh Sagili
Rachael Winfree

Participants Attachment:

NC1173 meeting minutes 2024.docx

Brief Summary of Minutes

Brief Summary of Annual NC1173 Multi-State Project Meeting

Minutes were taken by Priya Basu (Mississippi State University)

List of attendees in person: Priya Chakrabarti Basu, Margarita López-Uribe, Judy Wu-Smart, Kate Anton (for Christina Grozinger), Ana Heck, Robyn Underwood, Jamie Ellis, Declan Schroeder, David Wick, Cameron Jack, Lewis Bartlett, Brock Harpur, Juliana Rangel, David R. Tarpy, Zachary Huang, Reed Johnson, Esmaeil Amiri, Hongmei Li-Byarlay and Michelle Flenniken

List of attendees via Zoom: Christine Hamilton, Jeffrey Harris, Brian Spiesman, Geoffrey Williams, Rachel Vannette, Hollis Woodard, Tania Kim, Ramesh Sagili and Rachael Winfree

The meeting minutes: Margarita presided over the meeting as chair. She rotated off and vice-chair Priya is now the new Chair. Brock is the new vice-chair. NC1173 currently has 41 members from 24 states. With the project renewal, we currently have 31 members from 17 states.

The director’s report gave a brief overview of NC1173 as one of the five regional associations. NC1173 focuses on multistate efforts for the project and not on individual efforts. All land grant universities receive hatch funds of which 25% must be spent for multistate activities. This year was the renewal year for NC1173. Margarita worked with NC1173 administrators and the members in submitting the project renewal. Brian already reviewed the proposal. The advisory review is still pending. By the end of March we will have a better idea about the revisions and have another three months for final submission and approval. The renewed proposal name will continue to be NC1173. The deadline to submit project report is January 29, 2024.

Judy asked whether reporting by region rather than institution was possible or not. Margarita indicated it will be hard as we will need regional representatives. Margarita will create a working spreadsheet to catalog all participants’ grants and publications. A consensus was to use the AAPA website for hosting multistate effort outcomes.

It was also suggested to alternate the NC1173 meeting location between ABRC and the International Pollinator Conference. So next year we will meet at Reno with ABF—the year after we will meet with the Internal Pollinator Conference in Montana.

There is now a new objective 3 on bee monitoring. It was also suggested that each year of the project, there can be a focus on each objective of the renewed NC1173. Suggestions were also included about having a mid-year retreat or zoom call to catch up on the progress of the project between participants from various universities.

Accomplishments

Objective 1a: (Biotic Stressors: Pests & Pathogens)  Honey bees are attacked by a large number of parasites and pathogens. Varroa destructor—an ectoparasitic mite that feeds on honey bees—is one of the deadliest pests currently facing the US beekeeping industry. Varroa mites transmit viruses within and between colonies, including deformed wing virus (DWV), which are often associated with overwinter losses of honey bee colonies. In addition, managed honey bees are threatened by bacterial (e.g., American and European Foulbrood) and eukaryotic pathogens (e.g., Vairimorpha) and other pests (e.g., small hive beetles). Growing evidence has demonstrated that some of these honey bee pathogens can be picked up by wild bees visiting shared floral resources with honey bees. This potential for pathogen transmission has raised concerns about the consequences that poor pest and disease management in honey bees may have on wild bee fauna.  Short-term Outcomes:   <ul> <li style="font-weight: 400;">Based on research on the benefits of propolis to honey bee health, a bee supply company (Premiere Bee Products LLC) is now selling deep Langstroth-style boxes with rough, grooved interior walls that stimulate colonies to construct a propolis envelope. The propolis envelope provides stability to the immune system and microbiome and helps lower disease loads.</li> <li style="font-weight: 400;">Offering queen producers training on knowledge and improved techniques about diagnostic tools that have allowed them to produce and commercialize healthier queens.</li> <li style="font-weight: 400;">Demonstration that increasing floral diversity reduces pathogen loads in honey bees and wild bees.</li> </ul> Outputs: <ul> <li style="font-weight: 400;">Experimental work demonstrating that the presence of honey bee colonies in soybean fields and prairies has no detectable impact on wild bee communities. Instead, wild bee communities are influenced by the composition of the surrounding landscape, with most species showing negative relationships with cropland cover (Toth, ISU).</li> <li style="font-weight: 400;">Discovery and characterization of pathogens in honey bees and wild bees (Ellis, UF; Hines, PSU; Rangel, TAMU).</li> <li style="font-weight: 400;">Characterization of the phenology of pests across different regions of the US. This information serves as a foundation for Varroa treatment models, aiding beekeepers in the future as a part of a holistic approach to control this pest (Jack, UF).</li> <li style="font-weight: 400;">Efficacy of treatments for nosemosis found that the available treatments failed to reduce spore prevalence and intensity in treated bees. These studies have identified an area in need of future research (Ellis and Jack, UF; Sagili R).</li> <li style="font-weight: 400;">Evidence that increasing floral diversity reduces pathogen loads in wild bees (Hines and Grozinger, PSU).</li> </ul> Activities: <ul> <li style="font-weight: 400;">Team of scientists described honey bee infection with amoebic disease leading to an amplified effort to screen honey bees for this poorly described pathogen and conduct in vitro tests to determine its pathogenicity to honey bees (Ellis and Jack, UF).</li> <li style="font-weight: 400;">Investigations of the role of thymol as an immune stimulator that can reduce viral loads (Flenniken, MSU).  </li> <li style="font-weight: 400;">Investigations to characterize honey bee host-virus interactions through experiments that evaluated the impact of sublethal virus infections on honey bee health, using flight distance as a quantitative proxy for overall health (Flenniken, MSU). </li> <li style="font-weight: 400;">Workshops and training opportunities for professional queen producers titled (Amiri, MSU).</li> <li style="font-weight: 400;">Ongoing research efforts to develop new chemical options for small hive beetle control (Bartlett, UGA).</li> <li style="font-weight: 400;">Continued collaborations with industry (Dalan Animal Health) to combine bee vaccines with supplemental feeding for honey bee pathogen control (Delaplane and Bartlett, UGA).</li> <li style="font-weight: 400;">Research on a new potential pest Tropilaelaps mite to better understand how they disperse within and between colonies (Williams, Auburn).</li> <li style="font-weight: 400;">Novel data on pathogen dynamics between managed and wild bees in agroecosystems indicating that pathogen spillover is highly context-dependent (López-Uribe, PSU).</li> </ul> Milestones: <ul> <li style="font-weight: 400;">If our renewal project is approved, our goal is to publish shared protocols for pathogen quantification in honey bees and wild bees to increase opportunities for meta-analyses of data collected across the United States. This is the main goal for our shared multi-state efforts for year 2025.</li> </ul>   Objective 1b: (Abiotic Stressors: Pesticides, Forage Availability, Nutrition) Major abiotic stressors contributing to honey bee health decline include pesticide exposure, malnutrition, and climatic instability. NC1173 members are assessing the effects of these interacting factors on bees and their pollination services through laboratory assays, field experiments and landscape-level data.  Short-term Outcomes:   <ul> <li style="font-weight: 400;">Launched Penn State Honey and Pollen Diagnostics Lab which allows beekeepers, growers, researchers, and the public to submit samples for DNA metabarcoding analysis (Grozinger, PSU). </li> <li style="font-weight: 400;">Training citizen scientists, 4H students, and USDA and USGS scientists on pollen hand collection and bee nutrition (Basu, MSU).</li> </ul> Outputs: <ul> <li style="font-weight: 400;">Demonstrated antagonistic effects of neonicotinoid insecticides and ectoparasitic mites on Apis mellifera health (Williams, Auburn).</li> <li style="font-weight: 400;">Studies demonstrating that bumble bee species vary in heat resilience with queens being especially susceptible, and humidity levels need to be considered in the impacts of heat waves on bees (Hines, PSU). </li> <li style="font-weight: 400;">Improved lists of optimal plants for bumble bees and our understanding of the macronutrient requirements across bees enable a predictive framework for selecting optimal foraging plants (Hines and Grozinger, PSU).</li> <li style="font-weight: 400;">Student training on data collection to understand how land management and climate change affect wild bee communities (Kim and Spiesman, KSU). </li> <li style="font-weight: 400;">Development of a mobile app for land owners and the general public for identifying bee pollinators (Kim and Spiesman, KSU).</li> <li style="font-weight: 400;">Demonstrated that land use and weather conditions have led to a decline in honey production over the last 50 years, which facilitated the identification of ecoregions, land use, and weather conditions associated with improved nutrition and honey production (Grozinger, PSU). </li> </ul> Activities: <ul> <li style="font-weight: 400;">Development of AI-based classifiers for bee species identification of wild and museum species. These tools will accelerate wild bee research by overcoming the taxonomic bottleneck for this type of research (Kim and Spiesman, KSU).</li> <li style="font-weight: 400;">Comparison of the thermal physiology of queen bumble bees between a species experiencing local declines (Bombus auricomus) and a species exhibiting continent-wide increases (B. impatiens) found limited ability to acclimate to temperature (Hines, PSU). </li> <li style="font-weight: 400;">Research project to test the effect of common insecticides on the reproductive quality of queens and their intergenerational effects. In addition, we investigated the effect of plastic queen cups on the physiology and growth of honey bee queens (Amiri, MSU).</li> <li style="font-weight: 400;">New studies on the effect of simultaneous exposure of bees to immune system stimulating thyme oil and the neonicotinoid insecticide, clothianidin (Fleinniken, MSU).</li> <li style="font-weight: 400;">Combination of DNA metabarcoding and biochemical methods to analyze the source and nutritional content of bee-collected pollen from diverse bee species (Grozinger, PSU).</li> <li style="font-weight: 400;">Investigations to determine how attractive nutritional supplements are to honey bees. Studies use caged worker bees with commercially available pollen substitutes (AP23, MegaBee, UltraBee) and wildflower pollen (Ellis and Jack, UF).</li> <li style="font-weight: 400;">Assessment of floral visitation in bumble bees across the season and years through DNA barcoding in pollen combined with macronutrient ratios of pollen were used to better understand optimal forage for supporting diverse bumble bee communities (Hines and Grozinger, PSU).</li> <li style="font-weight: 400;">Implementation of transcriptomic approaches to obtain molecular signatures of bee stressors across different landscapes (Hines and Grozinger, PSU).</li> <li style="font-weight: 400;">Investigated using a juvenile hormone analog to reduce varroa mite reproduction in worker brood (Huang, MSU).</li> </ul> Milestones: <ul> <li style="font-weight: 400;">If our renewal project is approved, our goal is to develop a database of pollen lipids, proteins, phytosterols and amino acids that is publicly available for researchers, policymakers, citizens, and stakeholders. This is the main goal for our shared multi-state efforts for year 2028.</li> </ul>   Objective 2: (Genetics, Breeding, & Diversity) Breeding mite and disease resistant traits in honey bee stock and diversifying honey bee genetics and selection efforts are more sustainable solutions to address the pest and pathogen issues in honey bees and is a long-term goal for NC1173 members.   Short-term Outcomes: <ul> <li style="font-weight: 400;">Breeding-focused training events with beekeepers. Most attendees report an increase in knowledge of basic breeding skills that is likely to change their management practice as a result of training (Harpur, Purdue).</li> </ul>  Outputs: <ul> <li style="font-weight: 400;">Developed a new standardized test for AHB and a centralized testing facility. We have already sequenced 2,000 honey bees from 38 states using this platform (Harpur, Purdue; López-Uribe, PSU).</li> <li style="font-weight: 400;">Combined transcriptomics, genomics, and selective breeding using instrumental insemination for assisted breeding programs (Harpur, Purdue).</li> <li style="font-weight: 400;">Using controlled reciprocal crosses, genome sequencing, and transcriptomics, new data demonstrates that genes inherited from the mothers and fathers have differential effects on bee behavior and physiology (Grozinger, PSU).</li> </ul>  Activities: <ul> <li style="font-weight: 400;">Active selection programs of breeds that resist the Varroa mites have resulted in over 100 colonies that have survived at least one winter without treatments (Spivak, UMN). </li> <li style="font-weight: 400;">Testing whether colonies that express hygienic behavior show resistance to Deformed Wing Virus (Spivak, and Schroeder, UMN).</li> </ul>  Milestones: <ul> <li style="font-weight: 400;">If our renewal project is approved, the main milestone for this objective is to review the available information on honey bee stock in the United States and their phenotypic traits. This information will be shared via a peer-reviewed publication and extension materials. This is the main goal for our shared multi-state efforts for year 2026. </li> </ul>   Objective 3: (Management)  Management practices to maintain healthy honey bees and landscapes that support pollinators are in high demand and recommendations continue to evolve with new research. Therefore, NC1173 members strive to engage in research activities that are relevant to stakeholder needs to better provide the most up-to-date, science-based recommendations to beekeepers, pesticide applicators, farmers, homeowners, and policymakers. Efforts for this objective include recommendations on how to better manage pests and pathogens in honey bees, enhancing landscapes for pollinators, and options to reduce exposure or mitigate the effects of pesticides.   Short-term Outcomes:   <ul> <li style="font-weight: 400;">Major revision of the Beekeeping in Northern Climates short course manual and online course. This material is freely available online (Spivak, UMN).</li> <li style="font-weight: 400;">Education of beekeepers on how to induce a summer brood break as a tool for Varroa control (Bartlett, UGA).</li> <li style="font-weight: 400;">Expansion of Beescape decision support tool to help beekeepers, growers, conservationists, and the public manage landscapes to improve bee health (Grozinger, PSU).</li> <li style="font-weight: 400;">Learning of beekeeping basic techniques to control pests, 80% of participating beekeepers expressed that they intend to implement learned knowledge, and 58% thought the information they learned would save them more than $50 (Williams, Auburn).</li> </ul>  Outputs: <ul> <li>Honey bees experience positive health effects (increased bee population and colony weight) when they live near prairie strips integrated into crop fields compared to crop fields without these landscape enhancements (Toth, ISU).</li> <li>Increased flower resources in natural habitats produced a nested network supporting higher bee richness and a greater chance for bee-mediated plant pollination. Some bee groups showed improved health indicators at prairie strip sites and these may be influenced by evolutionary family, foraging preferences, and body size (Toth, ISU). </li> <li>Statistics reporting national losses and drivers of honey bee losses in the United States (Williams, Auburn).</li> <li>Cass et al. conducted surveys of farmers, landowners, and beekeepers and summarized the findings in an article recently accepted at the Journal of Integrated Pest Management. Overall, we document strong support and enthusiasm for pollinator-friendly practices in Iowa, but note gaps in knowledge about which practices are most effective and what tools are available to implement them. These results suggest a way for pollinator extension programs to address these knowledge gaps in a receptive group of beekeepers, farmers, and landowners.</li> <li>Hosted practical workshops with a focus on IPM tools for beekeeping. This was a coordinated online beekeeping webinar called “At Home Beekeeping” with participation from 12 institutions (Auburn, UF, UGA, U Tennessee, NCSU, KSU, MSU, LSU, TAMU, USDA-ARS, USDA-ARS Stoneville, USDA-ARS Baton Rouge, USDA-ARS Poplarville).</li> <li>Development of optimal organic beekeeping management practices for stationary beekeeping operations in the northeast (López-Uribe, PSU)</li> <li>Quarterly column in American Bee Journal demystifying misunderstandings about organic beekeeping management (López-Uribe, PSU)</li> </ul>  Activities: <ul> <li>Coordinated efforts to assess winter capped brood monitoring (https://aub.ie/winterbrood) (UF, UGA, MSU, U Tennessee, TAMU, USDA-ARS, OSU, Cornell, Central State, PSU)</li> <li>Updated the Beescape decision support tool based on survey responses from beekeepers, growers, conservationists, and scientists. The fool now allows for more flexible analyses and provides the economic value of pollination services to crops (Grozinger, PSU).</li> <li>Development of unique beekeeping support systems for hobby and commercial beekeepers in MN and the North Central region (Spivak, UMN).</li> <li>Collected a large data set on the native bee species found in forests of different successional ages. In addition to the bee species, pollen collected from hundreds of bee specimens was also identified (Winfree, Rutgers).</li> </ul> Milestones: <ul> <li style="font-weight: 400;">If our renewal project is approved, the main milestone for this objective is to two-fold. First, we aim to develop a centralized repository with documents about best management practices for honey bees and landscapes for different regions across the United States; and (2) make publicly available general recommendations for plant species (e.g., seed mixes) and their nutritional value to wild and managed bees. These are the main goals for our shared multi-state efforts for year 2029. </li> </ul>

Publications

Summary table and list of publications by topic reported by NC1173 committee members for 2023. NC1173 authors are indicated in bold. <table> <tbody> <tr> <td> Publications by topic </td> <td> 2023 </td> </tr> <tr> <td> Obj 1a: Biotic (Pests & pathogens) </td> <td> 11 </td> </tr> <tr> <td> Obj 1b: Abiotic (Pesticides, nutrition, landscapes)  </td> <td> 10 </td> </tr> <tr> <td> Obj 2: Genetics, Breeding, Diversity </td> <td> 5 </td> </tr> <tr> <td> Obj 3: Management </td> <td> 16 </td> </tr> <tr> <td> Other Publications </td> <td> 10 </td> </tr> <tr> <td> Total </td> <td> 52 </td> </tr> <tr> <td> Publications with >1 NC1173 authors </td> <td> 16 </td> </tr> </tbody> </table> Objective 1a: Biotic Stressors (Pests & pathogens) Clair ALS, Zhang G, Dolezal AG, O’Neal ME, Toth AL (2023) Agroecosystem landscape diversity shapes wild bee communities independent of managed honey bee presence Agriculture, Ecosystems & Environment 327, 107826 Dickey M, Whilden M, Twombly Ellis J, Rangel J (2023) A preliminary survey reveals that common viruses are found at low levels in a wild population of honey bees (Apis mellifera). Journal of Insect Science. 23(6): 26; 1–11. Gratton EM, McNeil DJ, Grozinger CM, Hines HM. (2023) Local habitat type influences bumble bee pathogen loads and bee species distributions” Environmental Entomology 52 (3), 491-501 <a href="https://doi.org/10.1093/ee/nvad027">https://doi.org/10.1093/ee/nvad027</a> Iredale ME, Viadanna PHO, Subramaniam K, Tardif E, Bonning BC, Ellis JD. Report of amoebic disease in a colony of Western honey bees (Apis mellifera). Veterinary Pathology, 2023;60(5): 709-713. https://doi.org/10.1177/03009858231179956.  Jack CJ, Oliveria IdB, Kimmel CB, Ellis JD. Seasonal differences in Varroa destructor population growth in western honey bee (Apis mellifera) colonies. Frontiers in Ecology and Evolution, 2023;11:1102457. https://doi.org/10.3389/fevo.2023.1102457.  Liu J, Zhang R, Tang R, Zhang Y, Guo R, Xu G, Chen D, Huang ZY, Chen Y, Han R, Li, W. The role of honey bee derived aliphatic esters in the host-finding behavior of Varroa destructor. Insects 2023, 14, no. 1: 24. <a href="https://doi.org/10.3390/insects14010024">https://doi.org/10.3390/insects14010024</a> Orlova M., Porter M, Hines HM, Amsalem E. Symptomatic infection with Vairimorpha bombi decreases diapause survival in wild bumble bee species (Bombus griseocollis). Animals 2023;13 (10):1656 Powell JE, Lau P, Rangel J, Arnott R, DeJong T, Moran NA (2023) The microbiome and gene expression of honey bee workers are affected by a diet containing pollen substitutes. PLoS ONE. 18(5): e0286070. https://doi.org/10.1371/journal.pone.0286070  Prouty C, Jack C, Sagili R, Ellis JD. Evaluating the efficacy of common treatments for Vairimorpha (Nosema) spp. control. Applied Sciences, 2023;13(3): 1303. <a href="https://doi.org/10.3390/app13031303">https://doi.org/10.3390/app13031303</a>. Ray AM, Gordon EC, Seeley TD, Rasgon JL, Grozinger CM. (2023) Signatures of adaptive decreased virulence of deformed wing virus in an isolated population of wild honey bees (Apis mellifera). Proceedings of the Royal Society B 290(2009). https://doi.org/10.1098/rspb.2023.196.  Wen P, Chen J, Huang ZY. (2023). Death recognition by undertaker honey bees based on reduced cuticular hydrocarbon emissions. Entomologia Gereralis. DOI: 10.1127/entomologia/2023/1607   Objective 1b: Abiotic Stressors (Pesticides, nutrition, landscapes) Bruckner S, Straub L, Neumann P, Williams GR. (2023) Negative but antagonistic effects of neonicotinoid insecticides and ectoparasitic mites Varroa destructor on Apis mellifera honey bee food glands. Chemosphere 313:137535. <a href="https://doi.org/10.1016/j.chemosphere.2022.137535">https://doi.org/10.1016/j.chemosphere.2022.137535</a> Chakrabarti P, Sagili RR. Managed foraging for honey and crop pollination – Honey bees as livestock. Chapter 8 in the book The Foraging Behavior of the Honey Bee (Apis mellifera L.). 2023:175–193. Edited by John Purdy, Elsevier Academic Press, ON, Canada.  Crone M, Boyle N, Bresnahan S, Biddinger D, Richardson R, Grozinger CM. (2023) More than mesolectic: Characterizing the nutrition niche of Osmia cornifrons” Ecology and Evolution 13(10), e10640. https://doi.org/10.1002/ece3.10640. Feuerborn, C., Quinlan, G., Shippee, R., Strausser, T.L., Terranova, T., Grozinger CM, Hines HM. (2023) Variance in heat tolerance in bumble bees correlates with species geographic range and is associated with several environmental and biological factors” Ecology and Evolution 13, e10730. https://doi.org/10.1002/ece3.10730.  Lau P, Sgolastra F, Williams GR, Straub L. (2023) Editorial: Insect pollinators in the Anthropocene: How multiple environmental stressors are shaping pollinator health. Front Ecol Evol. 2023;11:1279774 https://doi.org/10.3389/fevo.2023.1279774. Lau PW, Esquivel IL, Parys KA, Hung K-LJ, Chakrabarti P. (2023) The nutritional landscape in agroecosystems: a review on how resources and management practices can shape pollinator health in agricultural environments. Annals of the Entomological Society of America:1-15. Manaswi A, Noordyke E, Prouty C, Ellis JD. (2023) Western honey bee (Apis mellifera L.) attraction to commercial pollen substitutes and wildflower pollen in vitro. Journal of Applied Research 147: 244-247. <a href="http://dx.doi.org/10.1111/jen.13102">http://dx.doi.org/10.1111/jen.13102</a>.  Quinlan GM, Miller DAW, Grozinger CM (2023) Examining spatial and temporal drivers of pollinator nutritional resources: Evidence from five decades of honey bee colony productivity data. Environmental Research Letters 18(11): 114018 DOI 10.1088/1748-9326/acff0c  Quinlan GM, Grozinger CM (2023) Honey bee nutritional ecology: From physiology to landscapes. Advances in Insect Physiology https://doi.org/10.1016/bs.aiip.2023.01.003.  Quinlan GM, Feuerborn C, Hines HM, Grozinger CM (2023)Beat the heat: Thermal respites and access to food associated with increased bumble bee heat tolerance Journal of Experimental Biology 226 (17): jeb245924. doi: https://doi.org/10.1242/jeb.245924.    Objective 2: Genetics, Breeding, Diversity Bresnahan ST, Lee E, Clark L, Ma R, Rangel J, Grozinger CM, Li-Byarlay H (2023) Examining parent-of-origin effects on transcription and RNA methylation in mediating aggressive behavior in honey bees (Apis mellifera). BMC Genomics. <a href="https://doi.org/10.1186/s12864-023-09411-4">https://doi.org/10.1186/s12864-023-09411-4</a> Cambron-Kopco L, Underwood RM, Given JK, Harpur BA, López-Uribe MM. (2023) Honey bee stocks exhibit high levels of intra-colony variation in viral loads. J. Apic. Res. 1–4 doi:10.1080/00218839.2023.2285153  Gmel AI, Guichard M, Dainat B, Williams GR, Eynard S, Vignal A, Servin B, the Beestrong Consortium, and Neuditschko M. Identification of runs of homozygosity in western honey bees (Apis mellifera) using whole-genome sequencing data. Ecol Evol. 2023;13:e9723. <a href="https://doi.org/10.1002/ece3.9723">https://doi.org/10.1002/ece3.9723</a> Karlikow M, Amalfitano E, Yang X, Doucet J, Chapman A, Mousavi PS, Homme P, Sutyrina, P, Chan W, Lemak S, Yakunin, AF, Dolezal AG, Kelley S, Foster LJ, Harpur BA, Pardee K. CRISPR-induced DNA reorganization for multiplexed nucleic acid detection. Nature Communications. 2023; doi:10.1038/s41467-023-36874-6  Morfin N, Harpur BA, De la Mora A, Guzman-Novoa E. Breeding honey bees (Apis mellifera L.) for low and high Varroa destructor population growth: gene expression of bees performing grooming behavior. Frontiers in Insect Science. 2023; doi:10.3389/finsc.2023.951447   Objective 3: Management  Abou-Shaara HF, Jack CJ, Ellis JD. The impact of smoke and fogged/vaporized thyme oil on honey bee (Apis mellifera) survival and behavior in vitro. Journal of Apicultural Research, 2023;62(3): 643-645. <a href="https://doi.org/10.1080/00218839.2022.2135809">https://doi.org/10.1080/00218839.2022.2135809</a>. Bartlett LJ, Baker C, Bruckner S, Delaplane KS, Hackmeyer EJ, Phankaew C, Williams GR, Berry JA. (2023) No evidence to support the use of glycerol–oxalic acid mixtures delivered via paper towel for controlling Varroa destructor (Mesostigmata: Varroidae) mites in the Southeast United States. Journal of Insect Science 23(6):18. Berry JA, Braman SK, Delaplane KS, Bartlett LJ. 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. 2023 Nov 1;23(6):14. Borchardt KE, Kadelka C, Schulte LA, Toth AL (2023) An ecological networks approach reveals restored native vegetation benefits wild bees in agroecosystems. Biological Conservation 287, 110300. Browning AD,  Smitley D,  Studyvin J, Runkle ES, Huang ZY,  Hotchkiss E (2023). Variation in pollinator visitation among garden cultivars of marigold, portulaca, and bidens. Journal of Economic Entomology 116: 872–881 Cass RP, Hodgson EW, O’Neal ME, Toth AL, Dolezal AG (2023) Attitudes about honey bees and pollinator-friendly practices: a survey of Iowan beekeepers, farmers, and landowners. Journal of Integrated Pest Management 13 (1), 30.  Cruz SM, Grozinger CM. (2023). Mapping student understanding of bees: Implications for pollinator conservation. Conservation Science and Practice, 5( 3), e12902. https://doi.org/10.1111/csp2.12902 (2023). Hackmeyer EJ, Washburn TJ, Delaplane KS, Bartlett LJ. (2023) Successful application of anthranilic diamides in preventing small hive beetle (Coleoptera: Nitidulidae) infestation in honey bee (Hymenoptera: Apidae) colonies. Journal of Insect Science 23(6):12. Genung MA,  Reilly J, Williams NM, Buderi A, Gardner J, Winfree R (2023) Rare and declining bee species are key to consistent pollination of wildflowers and crops across large spatial scales. Ecology 104: e3899 https://doi.org/10.1002/ecy.3899 Petitta IR, López-Uribe MM, Sabo AE. (2023) Biology and management of wild lupine (Lupinus perennis L.): a case study for conserving rare plants in edge habitat. Plant Ecology  [link] Prestby TJ, Robinson AC, McLaughlin D, Dudas PM, Grozinger CM. (2023)“Characterizing user needs for Beescape: A spatial decision support tool focused on pollinator health” Journal of Environmental Management 325: 116416 (2023). <a href="https://doi.org/10.1016/j.jenvman.2022.116416">https://doi.org/10.1016/j.jenvman.2022.116416</a> Prouty C, Abou-Shaara HF, Stanford B, Ellis JD, Jack C. (2023) Oxalic acid application method and treatment intervals for reduction of Varroa destructor populations in western honey bee (Apis mellifera) colonies. Journal of Insect Science. 23(6): 13.  Prouty C, Jack C, Sagili R, Ellis JD. (2023) Evaluating the efficacy of common treatments used for Vairimorpha (Nosema) spp. Control. Applied Sciences. 13(3): 1303. Underwood RM, Lawrence B, Turley NE, Cambron-Kopco L, Kietzman P, Traver BE, López-Uribe MM. (2023) A longitudinal experiment demonstrates that organic beekeeping management systems support healthy and productive honey bee colonies. Scientific Reports 13(1): 6072 Weinman LR, Ress T, Gardner J, Winfree R. (2023). Individual bee foragers are less efficient transporters of pollen for the plants from which they collect the most pollen into their scopae. American Journal of Botany DOI: 10.1002/ajb2.16178  Zhang G, Murray CJ, Clair AL, Cass RP, Dolezal AG, LA Schulte, O’Neal ME, Toth AL (2023) Native vegetation embedded in landscapes dominated by corn and soybean improves honey bee health and productivity. Journal of Applied Ecology 60 (6), 1032-1043   Other peer-reviewed publications Bresnahan ST, Galbraith D, Ma R, Anton K, Rangel J, Grozinger CM (2023) Beyond conflict: Kinship theory of intragenomic conflict predicts individual variation in altruistic behaviour. Molecular Ecology. https://doi.org/10.1111/mec.17145  Freitas F, Branstetter M, Franceschini-Santos V, Dorchin A, Wright K, López-Uribe MM, Griswold T, Silveira F, Almeida E. (2023). UCE phylogenomics, biogeography, and classification of long-horned bees (Hymenoptera: Apidae: Euceerini), with insights on using specimens with extremely degraded DNA. Insect Systematics and Diversity 7(4):3 Gutierrez GM, LeCroy LA, Roulston TH, Biddinger DJ, López-Uribe MM. (2023) Osmia taurus (Hymenoptera: Megachilidae): A new non-native bee species with invasiveness potential in North America. Environmental Entomology 52(2):149–156 Han B, Amiri E, Wei Q, Tarpy DR, Strand MK, Xu S, Rueppell O. Group size influences maternal provisioning and compensatory larval growth in honeybees. Iscience. 2023 Dec 15;26(12). Miles GP, Liu XF, Amiri E, Grodowitz MJ, Allen ML, Chen J. Co-Occurrence of wing deformity and impaired mobility of alates with Deformed Wing Virus in Solenopsis invicta Buren (Hymenoptera: Formicidae). Insects. 2023 Sep 27;14(10):788. Mortensen AN, Ellis JD. (2023) Honey bees reared in isolation adhere to normal age-related division of labor when introduced into a colony. Applied Animal Behavior Science 258: 105824. <a href="https://doi.org/10.1016/j.applanim.2022.105824">https://doi.org/10.1016/j.applanim.2022.105824</a>. Pope N, Singh A, Childers A, Kapheim K, Evans J, López-Uribe MM. (2023) Expansion of agriculture drives adaptive evolution in a specialized squash pollinator. PNAS 120(15): e2208116120 Prouty C, Bartlett LJ, Krischik V, Altizer S. Adult monarch butterflies show high tolerance to neonicotinoid insecticides. Ecological Entomology. 2023 Apr 13. Rangel J, Lau P, Strauss B, Hildinger E, Hernandez B, Rodriguez S, Bryant V, Tarone AM (2023) A Texas population of blow flies (Diptera: Calliphoridae) highlights underappreciated aspects of their biology. Ecological Entomology. 1–10. https://doi.org/10.1111/een.13298  Sandoval-Arango S, Branstetter M, Cardoso C, López-Uribe MM. (2023). Phylogenomics reveals within species diversification but incongruence with color phenotypes in widespread orchid bees (Hymenoptera: Apidae: Euglossini). Insect Systematics and Diversity 7(2):1-13   Non peer-reveiwed publications Anton K, Darnell C, Grozinger CM, Underwood R. “An Introduction to Honey Bee Breeding Program Design”. Penn State Extension. 2023 https://extension.psu.edu/an-introduction-to-honey-bee-breeding-program-design <a href="https://pollinators.psu.edu/news/honey-bees-may-inherit-altruistic-behavior-from-their-mothe">https://pollinators.psu.edu/news/honey-bees-may-inherit-altruistic-behavior-from-their-moth</a> Bruckner S, López-Uribe MM, Underwood RM (2023) Organic and Treatment-free Colony Management – They are not the same. American Bee Journal 163(10):1123-1125. Chakrabarti, P. Young Zoologist - Honey Bees. neon Squid Books, McMillan Publishers, London. Delaplane K, Hudson W, Johnson A. Yellow-Legged Hornet. UGA Extension bees.caes.uga.edu Dickey M*, Rangel J (2023) Comparative quantification of honey bee (Apis mellifera) associated viruses in wild and managed colonies. In: López-Uribe MM, Chakrabarti P, Harpur BA (eds.) Proceedings of the 2023 American Bee Research Conference. Bee Culture. A <a href="https://doi.org/10.55406/ABRC.23">https://doi.org/10.55406/ABRC.23</a> Lee K, Reuter GS, Spivak M. Beekeeping in Northern Climates. Third Edition. University of Minnesota Extension. 2024 <a href="https://drive.google.com/file/d/1VCZSD89XPYtWmNn3vh9IypfGpNUMYics/view">https://drive.google.com/file/d/1VCZSD89XPYtWmNn3vh9IypfGpNUMYics/view</a> López-Uribe MM, Chakrabarti P, Harpur BA, Rangel J, Goblirsch M, Underwood R (2023) Introduction to the Proceedings. In: López-Uribe MM, Chakrabarti,P., Harpur, BA (eds.) Proceedings of the 2023 American Bee Research Conference. Bee Culture. A <a href="https://doi.org/10.55406/ABRC.23">https://doi.org/10.55406/ABRC.23</a> López-Uribe MM, Underwood RM, Bruckner S (2023) The benefits of organic beekeeping and how management affects honey bee colony health, survival, and productivity. American Bee Journal 163(7):753-755. Rangel J, Fei C, Chen Y, Woodward R (2023) Market implications of changes in climate, land coverage and annual colony loss rates for U.S. commercial beekeeping operations. In: López-Uribe MM, Chakrabarti P, Harpur BA (eds.) Proceedings of the 2023 American Bee Research Conference. Bee Culture. A https://doi.org/10.55406/ABRC.23  Rangel J, Pino M (2023) Food 4 Farmers: A nonprofit organization working with coffee growers in Latin America on beekeeping and alternative farming activities to overcome food insecurity during the “thin” months. American Bee Journal. 163(11): 1227-1230.  Smith D, Rangel J, Bouga M, Parejo M (2022 and 2023) Special issue on stingless bees. Journal of Apicultural Research. 61(5): 577-577, https://doi.org/10.1080/00218839.2022.2122307  Toth, A. 2023. Honey bees: Good guys or bad guys? Beeline (Newsletter of the Central Iowa Beekeepers' Association), Spring 2023 Issue. Twombly Ellis J*, Rangel J (2023) Pesticide stress drives premature self-removal behavior in honey bee (Apis mellifera) workers. In: López-Uribe MM, Chakrabarti,P., Harpur, BA (eds.) Proceedings of the 2023 American Bee Research Conference. Bee Culture. A https://doi.org/10.55406/ABRC.23 [25]  Vu AT, Ellis JD. 2023. Episode 130: Controlling Varroa Through Genetic Technology. Two Bees in a Podcast. https://podcasters.spotify.com/pod/show/ufhbrel  Vu, A.T., Ellis, J.D. 2023. Episode 127: Varroa Control Methods in Ontario. Two Bees in a Podcast. <a href="https://podcasters.spotify.com/pod/show/ufhbrel">https://podcasters.spotify.com/pod/show/ufhbrel</a> Vu, A.T., Ellis, J.D. 2023. Episode 131: Follow-up on Microplastics. Two Bees in a Podcast. <a href="https://podcasters.spotify.com/pod/show/ufhbrel">https://podcasters.spotify.com/pod/show/ufhbrel</a>  Vu AT, Ellis JD. 2023. Episode 135: Shipping Queen Cells. Two Bees in a Podcast. <a href="https://podcasters.spotify.com/pod/show/ufhbrel">https://podcasters.spotify.com/pod/show/ufhbrel</a>  Vu AT, Ellis JD. 2023. Episode 147: Generational Beekeeping and Queen Breeding with Ted Miksa. Two Bees in a Podcast. <a href="https://podcasters.spotify.com/pod/show/ufhbrel">https://podcasters.spotify.com/pod/show/ufhbrel</a>  Vu AT, Ellis JD. 2023. Episode 149: Drones Galore! Two Bees in a Podcast. <a href="https://podcasters.spotify.com/pod/show/ufhbrel">https://podcasters.spotify.com/pod/show/ufhbrel</a>

Impact Statements

Supporting healthier managed and wild pollinators is critical for ecosystem function and sustainable agriculture. To help advance our knowledge and develop potential strategies to mitigate the multiple stressors that pollinator populations face, members of the NC1173 research group have made significant progress in gaining a fundamental understanding of the impact of biotic and abiotic stressors and their interactions on pollinator health. Additionally, efforts on fundamental and applied research have allowed for the incorporation of breeding and management tools to help mitigate the negative impacts of these stressors. Knowledge about these research advances has been transferred to a diverse group of targeted stakeholders that include: beekeepers, farmers, landowners, and the general public. All of these efforts have helped bring awareness about bees, their role and the challenges they are facing, and have facilitated changes in (1) land management practices that offer better nutrition and lower pathogen risk for pollinators, (2) safer pesticide application methods that help mitigate other stressors (e.g., climate and pathogens pressure), (3) beekeeping management practices that rely less on synthetic chemical treatments, and (4) access to regional educational programs that can support better decision making on how to support healthier bee populations. Additionally, our team is supporting the training of the next generation of professionals who will continue to work on issues related to bee health. Overall, the research and education programs led by this team are providing critical information to improve managed and wild pollinator health across the U.S.