Source: CORNELL UNIVERSITY submitted to NRP
FUNGICIDES AND POLLINATOR HEALTH: QUANTIFYING MECHANISMS OF STRESS TO INFORM REAL WORLD SOLUTIONS
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
COMPLETE
Funding Source
AFRI COMPETITIVE GRANT
Reporting Frequency
Annual
Accession No.
1019014
Grant No.
2019-67013-29561
Cumulative Award Amt.
$499,000.00
Proposal No.
2018-08603
Multistate No.
(N/A)
Project Start Date
May 15, 2019
Project End Date
May 14, 2024
Grant Year
2019
Program Code
[A1113]- Pollinator Health: Research and Application
Recipient Organization
CORNELL UNIVERSITY
(N/A)
ITHACA,NY 14853
Performing Department
Entomology
Non Technical Summary
A growing number of studies are finding surprisingly strong links between fungicides and wild and managed bee health. These studies mirror concern from commercial beekeepers, who consistently say that more research is needed to understand risk posed from fungicide exposure during crop pollination. Because fungicides are relatively non-toxic to bees, risk is generally determined to be low via current Risk Quotient (RQ) measures. However, the two dominant hypothesized mechanisms for how fungicides are impacting bees - synergisms with insecticides and increased susceptibility to parasites - are not currently accounted for in RQ estimates. Furthermore, risk is rarely considered for multiple bee species, even though species-specific responses are common in response to pesticide and parasite stress. Here, we propose a new fungicide risk protocol that incorporates fungicide-insecticide and fungicide-parasite interactions, then apply it during pollination of apple, a major pollination-dependent crop in the United States. We will gather pesticide exposure and parasite prevalence data from 3 managed bee species and 10 focal taxa of wild bees across 20 commercial apple orchards. Based on exposure and prevalence, we will then conduct fungicide-insecticide and fungicide-parasite bioassays to measure potential effects with 6 species of wild and managed bees. These exposure and effect data will produce, to our knowledge, the broadest fungicide risk assessment for pollinators to date. Finally, for high-risk fungicides, we will assess the efficacy of multiple risk mitigation strategies, thereby evaluating strategies to increase pollinator health. Such strategies will provide long-range improvement in and sustainability of U.S. agriculture and food systems.
Animal Health Component
50%
Research Effort Categories
Basic
50%
Applied
50%
Developmental
(N/A)
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
2113010115025%
2113085115045%
2121110115010%
1363085107010%
2041110107010%
Knowledge Area
212 - Pathogens and Nematodes Affecting Plants; 204 - Plant Product Quality and Utility (Preharvest); 211 - Insects, Mites, and Other Arthropods Affecting Plants; 136 - Conservation of Biological Diversity;

Subject Of Investigation
1110 - Apple; 3010 - Honey bees; 3085 - Other bees (non-Apis bees) - All bees except Apis cerana; includes Bombas, Alfalfa leaf-cutter;

Field Of Science
1070 - Ecology; 1150 - Toxicology;
Goals / Objectives
Objective 1. Determine parasite prevalence and field exposure to fungicides and insecticides during apple pollination for 10 focal taxa (6 genera) of wild bees and 3 species of managed bees.Objective 2. Determine which fungicide-insecticide combinations and which fungicide-parasite interactions lead to increased mortality of bees.Objective 3. Determine whether high-risk fungicides attract or deter bees, and test how different spray practices and putatively deterrent adjuvants may be used to limit fungicide risk while interfering minimally with pollination and plant pathogen control.
Project Methods
Objective 1. Determine parasite prevalence and field exposure to fungicides and insecticides during apple pollination for 10 focal taxa (6 genera) of wild bees and 3 species of managed bees. We will utilize a network of 20 New York State apple orchards that vary in spray practices and pesticide risk to bees (Park et al. 2015; McArt et al. 2017a, Centrella et al. in prep) to assess pesticide exposure, parasite prevalence, and pesticide-parasite covariation within 10 focal wild bee taxa and 3 managed bees. Importantly, we have recently improved our multi-residue pesticide analysis from 30 compounds to 294 compounds, greatly expanding the scope of our pesticide detection capabilities. At the same time, we have optimized a 5-parasite multiplex PCR assay to rapidly screen for parasites that we commonly find in both wild and managed bees. The pesticide and parasite data will be used to inform which parasites, fungicides, and fungicide-insecticide combinations are tested in bioassays described in Obj. 2.Objective 2. Determine which fungicide-insecticide combinations and which fungicide-parasite interactions lead to increased mortality of bees. We will conduct larval or adult bioassays with honey bees (Apis mellifera), bumble bees (Bombus impatiens), mason bees (Osmia cornifrons) and 3 of the 10 focal taxa of field-collected wild bees to assess the effects of fungicide-insecticide and fungicide-parasite interactions. We have experience conducting bioassays on the managed bees and have recently developed a protocol and completed laboratory bioassays on adult wild bees (see Objs. 2a & b). Furthermore, we have access to sufficient quantities of the wild bees, thus facilitating this diverse array of bioassays. Fungicide-insecticide bioassays will focus on compounds that are frequently found in combination and/or contribute to greatest exposure as determined in Obj. 1. Fungicide-parasite bioassays will focus on compounds and parasites that are frequently found to covary within particular bee species or among orchards. Results of the bioassays will inform which fungicides are assessed further for potential risk mitigation in Obj. 3.Objective 3. Determine whether high-risk fungicides attract or deter bees, and test how different spray practices and putatively deterrent adjuvants may be used to limit fungicide risk while interfering minimally with pollination and plant pathogen control. We will conduct choice assays using honey bees (Apis mellifera) and mason bees (Osmia cornifrons) to assess attraction of the bees to high-risk fungicides, and whether potential deterrent adjuvants can reduce attraction and exposure. For promising adjuvants, we will test whether the adjuvant interferes with fungal plant pathogen control and/or pollination services of apple via laboratory bioassays and manipulative field experiments. Finally, using field trials, we will test whether exposure to high-risk attractive fungicides can also be reduced via alternative spray practices, in particular spraying in the evening when bees will not forage for >10 hours post-spray.

Progress 05/15/19 to 05/14/24

Outputs
Target Audience:Target audiences reached during the project include beekeepers, veterinarians, farmers, pollinator health researchers, and regulators at the EPA and USDA. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?The two PhD students and postdoc funded by this project gave multiple talks at the American Bee Research Conference (ABRC) and the Entomological Society of America (ESA) throughout the project. The postdoc secured a job in industry (at BASF). How have the results been disseminated to communities of interest?Results have been disseminated via peer-reviewed publications, extension guides, and talks to beekeepers, growers, and researchers. In addition, McArt has shared results with the NYS Dept of Agriculture and Markets, agriculture advisors to the governor, and regulators at the EPA. What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? Our main paper summarizing Obj 1 was published in the Journal of Applied Ecology (see Mueller et al. 2024 J. Applied Ecol) and a second manuscript is currently in review (Zhao et al. in review). Briefly, we found that exposure to pesticides during crop pollination varies among bee species, and that honey bees are generally exposed to the highest-risk insecticides, possibly from foraging outside of apple orchards and being exposed to neonicotinoids from seed treatments on corn or soybean seeds during planting. We published our first paper summarizing Objective 2 (De Souza et al. 2024 Sci. Reports) and we have another paper currently in review (Sanchez et al. in review). Brief summary: We conducted in vitro larval honey bee trials to assess whether interactions occurred between the insecticides thiamethoxam or acetamiprid and the fungicides mancozeb, cyprodinil, fluxapyraxad, difenoconazole, and captan. Exposure to all investigated pesticides reduced bee survival in at least one of the dose levels or when combined across dose levels. Some fungicides, particularly captan and difenoconazole, had effect sizes comparable to the insecticides. No general pattern of interactions was observed across fungicide-insecticide pairs, though we observed significant antagonism at all dose levels in the pair mancozeb-acetamiprid. All other pairs either showed no significant interactions or significant synergism/antagonism at only some dose levels. We found significant sublethal reductions in body weight of emerged adults for the fungicides mancozeb (all dose levels), cyprodinil (medium and high dose levels) and difenoconazole (super high dose level), and the insecticide thiamethoxam (all dose levels). None of the individual pesticides showed significant effects on developmental time. Still, we found significant interactions for the combination of fluxapyroxad and thiamethoxam at low and medium doses for both body weight and developmental time. These results show that several fungicides commonly used during crop pollination are acutely toxic to honey bee larvae at field-realistic concentrations. More broadly, the results highlight the importance of assessing the toxicity of pesticides to early developmental stages of non-target organisms and understanding interactions between pesticides to improve the sustainability of pest management. We have alerted scientists at the EPA to these results, and will continue to share our results with this regulatory body as further work is published.

Publications

  • Type: Journal Articles Status: Published Year Published: 2024 Citation: Caserto, J. S., L. Wright, C. Reese, M. Huang, M. Salcedo, S. Fuchs, S. Jung, S. H. McArt and M. Ma. 2024. Ingestible hydrogel microparticles improve bee health after pesticide exposure. Nature Sustainability. https://doi.org/10.1038/s41893-024-01432-5


Progress 05/15/23 to 05/14/24

Outputs
Target Audience:Target audiences reached during this reporting period include beekeepers, veterinarians, farmers, pollinator health researchers, and regulators at the EPA and USDA. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?A PhD student funded by this project gave talks at the American Bee Research Conference (ABRC) and the Entomological Society of America (ESA). How have the results been disseminated to communities of interest?Results have been disseminated via peer-reviewed publications, extension guides, and talks to beekeepers, growers, and researchers. In addition, McArt has shared results with the NYS Dept of Agriculture and Markets, agriculture advisors to the governor, and regulators at the EPA. What do you plan to do during the next reporting period to accomplish the goals?We will continue to publish work that has resulted from this project, and we will share the work with stakeholders and the public.

Impacts
What was accomplished under these goals? Our main paper summarizing Obj 1 was published in the Journal of Applied Ecology (see Mueller et al. 2024 J. Applied Ecol). We also published our first paper summarizing Objective 2 (De Souza et al. 2024 Sci. Reports) and we have another manuscript in review that further summarizes results from Obj 2. Brief summary: We conducted in vitro larval honey bee trials to assess whether interactions occurred between the insecticides thiamethoxam or acetamiprid and the fungicides mancozeb, cyprodinil, fluxapyraxad, difenoconazole, and captan. Exposure to all investigated pesticides reduced bee survival in at least one of the dose levels or when combined across dose levels. Some fungicides, particularly captan and difenoconazole, had effect sizes comparable to the insecticides. No general pattern of interactions was observed across fungicide-insecticide pairs, though we observed significant antagonism at all dose levels in the pair mancozeb-acetamiprid. All other pairs either showed no significant interactions or significant synergism/antagonism at only some dose levels. We found significant sublethal reductions in body weight of emerged adults for the fungicides mancozeb (all dose levels), cyprodinil (medium and high dose levels) and difenoconazole (super high dose level), and the insecticide thiamethoxam (all dose levels). None of the individual pesticides showed significant effects on developmental time. Still, we found significant interactions for the combination of fluxapyroxad and thiamethoxam at low and medium doses for both body weight and developmental time. These results show that several fungicides commonly used during crop pollination are acutely toxic to honey bee larvae at field-realistic concentrations. More broadly, the results highlight the importance of assessing the toxicity of pesticides to early developmental stages of non-target organisms and understanding interactions between pesticides to improve the sustainability of pest management. We have alerted scientists at the EPA to these results, and will continue to share our results with this regulatory body as further work is published.

Publications

  • Type: Journal Articles Status: Published Year Published: 2024 Citation: Graham, K. K., S. H. McArt and R. Isaacs. 2024. High pesticide exposure and risk to bees in pollinator plantings adjacent to conventionally managed blueberry fields. Science of the Total Environment 922:171248. https://doi.org/10.1016/j.scitotenv.2024.171248
  • Type: Journal Articles Status: Published Year Published: 2024 Citation: Mueller, T. G., N. Baert, P. A. Mu�iz, D. E. Sossa, B. N. Danforth and S. H. McArt. 2024. Pesticide risk during commercial apple pollination is greater for honeybees than other managed and wild bees. Journal of Applied Ecology 61:1289-1300. https://doi.org/10.1111/1365-2664.14661
  • Type: Journal Articles Status: Published Year Published: 2024 Citation: Strang, C., S. Rondeau, N. Baert, S. H. McArt, N. Raine and F. Muth. 2024. Field agrochemical exposure impacts locomotor activity in wild bumblebees. Ecology e4310. https://doi.org/10.1002/ecy.4310
  • Type: Journal Articles Status: Published Year Published: 2024 Citation: De Souza, D., C. Urbanowicz, W. H. Ng, N. Baert, A. A. Fersch, M. L. Smith and S. H. McArt. 2024. Acute toxicity of the fungicide captan to honey bees and mixed evidence for synergism with the insecticide thiamethoxam. Scientific Reports 14:15709. https://doi.org/10.1038/s41598-024-66248-x


Progress 05/15/22 to 05/14/23

Outputs
Target Audience:Target audiences reached during this reporting period include beekeepers, veterinarians, and pollinator health researchers. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?In addition to the technician funded by this project, a postdoc and grad student have benefited from data collected from the project. They have each given talks to beekeeper and researcher audiences, including the American Bee Research Conference (ABRC), Entomological Society of America (ESA) and the International Conference for Pollinator Biology, Health, and Policy. How have the results been disseminated to communities of interest?Results have been disseminated via peer-reviewed publications, extension guides, and talks to beekeepers, growers, and researchers. In addition, McArt has shared results with the NYS Dept of Agriculture and Markets and agriculture advisors to the governor. What do you plan to do during the next reporting period to accomplish the goals?We will continue to analyze our data, summarize and publish the work in peer-reviewed journals and extension guides, and give talks at beekeeper, grower, and researcher venues.

Impacts
What was accomplished under these goals? We currently have a manuscript in review that focuses on Obj. 1. Briefly, to compare pesticide exposure and risk across wild and managed bees, we sampled the main bee groups present during bloom in 20 apple orchards, including managed honeybees (Apis mellifera), managed bumblebee workers (Bombus impatiens), wild mining bees (Andrena spp. and Andrena [Melandrena] spp.), bumblebee foundress queens (Bombus impatiens), and eastern carpenter bees (Xylocopa virginica). We screened all bees for 92 pesticides and computed a Risk Quotient using available toxicity data (honeybee LD50s), adjusting for differences in toxicity known to scale with body mass. To gain insight into exposure origin, we compared residues in bees to those in focal orchard apple and dandelion flowers. Nearly all bee samples contained pesticides (97%), with the average contamination level ranging from 7.1±2.8 parts per billion (ppb) in B. impatiens workers to 388.4±146.2 ppb in Andrena. Exposure profiles were similar for all bees except A. mellifera, whose unique exposure profile included high levels of the neonicotinoid insecticide thiamethoxam. All bee groups except wild B. impatiens queens had at least one sample exceeding a U.S. Environmental Protection Agency or European Food Safety Authority exposure level of concern. A. mellifera experienced significantly greater risk than other bee groups, with 25% and 81% of samples exceeding an acute or chronic exposure level of concern, respectively. Risk to honeybees was driven primarily by high thiamethoxam levels not found in focal orchard flowers and likely originating outside the orchard. We find that pesticide exposure and risk differ between honeybees and other managed and wild bees during apple pollination. Furthermore, pesticide exposure is a landscape-scale phenomenon and therefore measures to reduce exposure must consider the surroundings beyond focal farms. Limiting orchard sprays, while reducing on-farm exposures, will not protect far-foraging bees from off-farm exposures such as thiamethoxam, which we hypothesize is coming from nearby seed-treated corn fields planted during apple bloom. In addition, we focused on Obj 2 during the current reporting period. We conducted in vitro larval honey bee trials to assess whether interactions occurred between the insecticides thiamethoxam or acetamiprid and the fungicides mancozeb, cyprodinil, fluxapyraxad, difenoconazole, and captan. Exposure to all investigated pesticides reduced bee survival in at least one of the dose levels or when combined across dose levels. Some fungicides, particularly captan and difenoconazole, had effect sizes comparable to the insecticides. No general pattern of interactions was observed across fungicide-insecticide pairs, though we observed significant antagonism at all dose levels in the pair mancozeb-acetamiprid. All other pairs either showed no significant interactions or significant synergism/antagonism at only some dose levels. We found significant sublethal reductions in body weight of emerged adults for the fungicides mancozeb (all dose levels), cyprodinil (medium and high dose levels) and difenoconazole (super high dose level), and the insecticide thiamethoxam (all dose levels). None of the individual pesticides showed significant effects on developmental time. Still, we found significant interactions for the combination of fluxapyroxad and thiamethoxam at low and medium doses for both body weight and developmental time. These results show that several fungicides commonly used during crop pollination are acutely toxic to honey bee larvae at field-realistic concentrations. More broadly, the results highlight the importance of assessing the toxicity of pesticides to early developmental stages of non-target organisms and understanding interactions between pesticides to improve the sustainability of pest management.

Publications

  • Type: Journal Articles Status: Published Year Published: 2023 Citation: Siviter, H., G. L. Pardee, N. Baert, S. H. McArt, S. Jha and F. Muth. 2023. Wild bees are exposed to low levels of pesticides in urban grasslands and community gardens. Science of the Total Environment 858:159839. https://doi.org/10.1016/j.scitotenv.2022.159839
  • Type: Journal Articles Status: Published Year Published: 2023 Citation: Bischoff, K., N. Baert, and S. H. McArt. 2023. Pesticide contamination of beeswax from 72 managed honeybee colonies in New York State. Journal of Veterinary Diagnostic Investigation 35:617-624. https://doi.org/10.1177/10406387231199098


Progress 05/15/21 to 05/14/22

Outputs
Target Audience:During the current reporting period, we gave 6 talks to academic audiences, 14 talks to extension audiences, and gave public testimony to the New York State Assembly Environment Committee regarding economic benefits and risk to pollinators from neonicotinoid insecticide usage in New York (NY). Academic audience talks Department of Entomology and Nematology, University of California, Davis, CA, May 2022 (via Zoom) Department of Entomology, University of California, Riverside, CA, April 2022 (via Zoom) Center for Environmental Policy, Bard College, Annandale-on-Hudson, NY, April 2022 (via Zoom) Department of Entomology, University of Illinois, Urbana-Champaign, IL, January 2022 (via Zoom) Department of Applied Ecology, North Carolina State University, Raleigh, NC, November 2021 School of Biological Science & Technology, Yangzhou University, China, June 2021 (via Zoom) Extension audience talks Massachusetts State Beekeepers Association Annual Conference, Essex, MA, March 2022 American Beekeeping Federation Annual Conference, Las Vegas, NV, January 2022 Apiary Inspectors of America Annual Conference, January 2022 (via Zoom) North Carolina State Beekeepers Association Annual Conference, Hickory, NC, November 2021 Northeastern IPM Center Advisory Council Annual Meeting, May 2021 (via Zoom) Honey Bee Health Coalition (Keystone Group, Colorado), May 2021 (via Zoom) Western NY Beekeepers Association, "Pesticides, pathogens, and pollinator declines: What we know and what YOU can do", Aurora, NY, May 2022 (25 people, 2 x 60 min talks) CCE Oswego Pollinator Health Workshop, "Pesticides, pathogens, and pollinator declines: What we know and what YOU can do", Zoom presentation, May 2022 (54 people, 60 min talk) NY Beekeeping Club President's Roundtable, "Research in the McArt lab and how to use the Cornell pesticide testing facility" Zoom presentation, March 2022 (15 people, 20 min talk) NY Cut Flower Growers Association, "Pesticides and bees: How to minimize risk to non-target organisms" Zoom presentation, January 2022 (32 people, 60 min talk) Empire State Honey Producers Association, "Update on what we know about pesticide exposure and risk to bees", "Varroa-mediated virus spillover from managed honey bees to wild bumble bees," Syracuse, NY, October 2021 (75 people, 2 x 60 min talks) NY Apiary Industry Advisory Committee, "Research update from Cornell" Zoom presentation, October 2021 (25 people, 30 min talk) NY Corn & Soybean Growers Association Board, "Neonicotinoid insecticides in field crops: Benefits to farmers and risk to bees" Zoom presentation, September 2021 (18 people, 45 min talk) New York Farm Bureau Advisory Board, "Neonicotinoid insecticides: When there are benefits to users and when there's risk to bees" Zoom presentation, August 2021 (18 people, 45 min talk) Public testimony to NYS Assembly Public testimony to the NYS Assembly regarding proposed legislation to restrict neonicotinoid insecticides in New York (September 20, 2021) https://nystateassembly.granicus.com/MediaPlayer.php?view_id=8&clip_id=6376 Changes/Problems:The pandemic severely impacted what was possible to accomplish on this project in 2020 and partially in 2021 and we are not in a position to complete Objective #3 as a result for staffing & budget reasons. Therefore, we will focus on completing Objectives #1 and #2 with remaining project funds. Both objectives have been very successful and we expect 4-5 additional peer-reviewed publications from this work. What opportunities for training and professional development has the project provided?The PhD student supported on this project (Tobias Mueller) presented his work at the January 2022 American Bee Research Conference and Cornell Entomology Graduate Student Symposium. Mueller, T.*, P. A. Muñiz, D. Sossa, N. Baert and S. H. McArt. Pesticide exposure during apple bloom differs between managed honey bees and wild native bees. American Bee Research Conference, Jan. 2022 (via Zoom). Mueller, T.*, P. A. Muñiz, D. Sossa, N. Baert and S. H. McArt. Pesticide exposure during apple bloom differs between managed honey bees and wild native bees. Cornell Entomology Graduate Student Symposium, Jan. 2022. How have the results been disseminated to communities of interest?During the current reporting period, results of this project have been disseminated via 6 talks to academic audiences, 14 talks to extension audiences, and public testimony to the New York State Assembly Environment Committee regarding economic benefits and risk to pollinators from neonicotinoid insecticide usage in NY. What do you plan to do during the next reporting period to accomplish the goals?During the next reporting period, we plan to finish writing the two papers from Obj. 1 that currently in manuscript form, as well as the two papers from Obj. 2 that currently in manuscript form. We plan to submit 4-5 manuscripts from this project in the next reporting period. In addition, we will continue to present our data at scientific conferences, academic visits, and extension events.

Impacts
What was accomplished under these goals? During the current reporting period, we completed a second year of sampling in 20 apple orchards to address Objective #1 and a second year of bioassays to address Objective #2. Because the pandemic severely impacted this project in 2020 and partially in 2021, we are not in a position to complete Objective #3. For Objective #1, during the current reporting period we collected samples of bees (5 focal taxa), soils, apple flowers, dandelions, honey bee-collected pollen, bumble bee wax, and mason bee pollen provisions from 20 farms. We analyzed all samples for 93 potential pesticide residues via LC-MS/MS in our chemical ecology core facility (https://blogs.cornell.edu/ccecf/). Overall, bumble bees were exposed to the greatest number of pesticides (average = 20 pesticides) while honey bees experienced greatest risk from exposure (honey bee-collected pollen from 11 of 20 farms exceeded the US Environmental Protection Agency level of concern for acute risk from contact exposure). We are currently writing up the results of these analyses for two peer-reviewed journals (Frontiers in Ecology & Evolution and Environmental Pollution). For Objective #2, we completed bioassays with honey bee larvae where we dosed larvae with 3 field-realistic concentrations of 6 fungicides (captan, mancozeb, difenaconazole, cyprodinil, fenbuconazole, fluxapyroxad) crossed with 2 field-realistic concentrations of 2 insecticides (acetamiprid, thiamethoxam). The most striking result from this work is that all six fungicides were acutely toxic to honey bee larvae at field-realistic doses. Some synergisms were observed with each insecticide, but overall the strength of synergisms was weaker than direct fungicide toxicity. We are currently writing up the results of these analyses for two peer-reviewed journals (Scientific Reports and Environment International).

Publications

  • Type: Journal Articles Status: Published Year Published: 2021 Citation: Chen, J., J. Webb, K. Shariati, S. Guo, J. K. Montclare, S. H. McArt and M. Ma. 2021. Pollen-inspired enzymatic microparticles to reduce organophosphate toxicity in managed pollinators. Nature Food 2:339-347. https://doi.org/10.1038/s43016-021-00282-0
  • Type: Journal Articles Status: Published Year Published: 2021 Citation: Graham, K. K., M. O. Milbrath, Y. Zhang, A. Soehnlen, N. Baert, S. H. McArt and R. Isaacs. 2021. Identities, concentrations, and sources of pesticide exposure in pollen collected by managed bees during crop pollination. Scientific Reports 11:16857. https://doi.org/10.1038/s41598-021-96249-z
  • Type: Journal Articles Status: Published Year Published: 2022 Citation: Graham, K. K., M. O. Milbrath, Y. Zhang, N. Baert, S. H. McArt and R. Isaacs. 2022. Pesticide risk to managed bees during blueberry pollination is primarily driven by off-farm exposures. Scientific Reports 12:7189. https://doi.org/10.1038/s41598-022-11156-1
  • Type: Journal Articles Status: Published Year Published: 2022 Citation: Rondeau, S., N. Baert, S. H. McArt and N. E. Raine. 2022. Quantifying exposure of bumblebee (Bombus spp.) queens to pesticide residues when hibernating in agricultural soils. Environmental Pollution 309:119722. https://doi.org/10.1016/j.envpol.2022.119722


Progress 05/15/20 to 05/14/21

Outputs
Target Audience:During the current reporting period we gave 18 talks to New York legislators (Senate and Assembly), the New York State (NYS) IPM program, the NYS Apiary Industry Advisory Committee, Cornell College of Veterinary Medicine Conservation Medicine Club, Finger Lakes Native Plant Society, York County Beekeepers Association (Pennsylvania), Inside The Hive TV, American Honey Producers Association Annual Conference, American Beekeeping Federation Annual Conference, Walworth County Beekeeping Club (Wisconsin), Montgomery County Beekeeping Club (Pennsylvania), Honey Bee Health Coalition (Keystone Group, Colorado), and Northeastern IPM Center Advisory Council Annual Meeting. In total, we reached approximately 750 stakeholders. Changes/Problems:The pandemic significantly impacted what we were able to accomplish in the lab regarding Objective 2. Given these major alterations, we may not be able to accomplish Objective 3 within the 3-yr time period of the grant. We are going to focus on Objective 2 for the next reporting period and assess what is feasible as we navigate the next year. What opportunities for training and professional development has the project provided?The postdoc on this project, Daiana De Souza, mentored one undergraduate (Christina Zhao) remotely during this reporting period. How have the results been disseminated to communities of interest?In addition to reaching approximately 750 people via talks, we also published one peer-reviewed paper and one extension publication during this reporting period. The extension publication, "Neonicotinoid insecticides in New York: Economic benefits and risk to pollinators", is 432 pages and is driving discussions on updated regulation of neonicotinoid insecticides in the state. What do you plan to do during the next reporting period to accomplish the goals?We are hoping we will not be as impacted by the pandemic during the next reporting period and will be able to accomplish more from Objective 2. Given the major alterations needed due to the pandemic, we may not be able to accomplish Objective 3 within the 3-yr time period of the grant.

Impacts
What was accomplished under these goals? During this reporting period we started working on Objective 2: Determine which fungicide-insecticide combinations and which fungicide-parasite interactions lead to increased mortality of bees. The pandemic significantly impacted what we were able to accomplish in the lab, but we started bioassays with honey bee larvae to look at the impact of captan (fungicide), mancozeb (fungicide), thiamethoxam (insecticide), acetamiprid (insecticide), and their interactions on larval development and mortality.

Publications

  • Type: Other Status: Published Year Published: 2020 Citation: Grout, T. A., P. A. Koenig, J. K. Kapuvari and S. H. McArt. 2020. Neonicotinoid insecticides in New York: Economic benefits and risk to pollinators. 432 pp. https://pollinator.cals.cornell.edu/pollinator-research-cornell/neonicotinoid-report/
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Chen, J., J. Webb, K. Shariati, S. Guo, J. K. Montclare, S. H. McArt and M. Ma. 2021. Pollen-inspired enzymatic microparticles to reduce organophosphate toxicity in managed pollinators. Nature Food 2:339-347. https://doi.org/10.1038/s43016-021-00282-0


Progress 05/15/19 to 05/14/20

Outputs
Target Audience:During this reporting period we gave 16 talks to the following groups: Cornell College of Veterinary Medicine Special Species Symposium, Caroline Elementary School, American Wildlife Conservation Foundation, Honey Bee Health for the Veterinarian 1-day workshop, Mann Library Chats in the Stacks, Cornell Reunion Weekend, Boyce Thompson Institute Summer REU program, Cornell Institute for Host-Microbe Interactions and Disease Summer REU program, Conservation Medicine One Health Summer program, Empire State Honey Producers Association Summer Picnic, Cornell Summer College Research Apprenticeship in Biological Sciences Program, NYS Department of Agriculture and Markets, Division of Animal Industry, NYS Veterinary Conference Honey Bee Track, Mid-York Beekeepers Association, Cornell Ag In-service day, Empire State Honey Producers Association, and the Greater New York Bee Conference. In total, we reached ~650 people at these events. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?One postdoc (Daiana De Souza) was hired on the project to coordinate field sampling and oversee analyses. Daiana will start to oversee Objective 2 next year. How have the results been disseminated to communities of interest?Yes, two peer-reviewed papers were published this reporting period. In addition, results were disseminated to ~650 stakeholders via talks and beekeeping meetings, environmental organizations, New York State (NYS) government advisory sessions, and several other venues. What do you plan to do during the next reporting period to accomplish the goals?The next reporting period will start to focus on bioassays for Obj. 2.

Impacts
What was accomplished under these goals? During the current reporting period we focused on Objective 1: Determine parasite prevalence and field exposure to fungicides and insecticides during apple pollination for 10 focal taxa (6 genera) of wild bees and 3 species of managed bees. We conducted a sampling of bees at 20 apple orchards in upstate New York. Across all orchards, we were able to focus on 4 genera of wild bees (Andrena, Melandrena, Xylocopa, Bombus), with several additional genera (Augochlora, Lasioglossum, Halictus) and a portion of the 20 sites. Each these bee species and several managed bees (Apis, Bombus, Osmia) and their hive matrices were analyzed for pesticide residues using our 93-pesticide multi-residue analysis.

Publications

  • Type: Other Status: Published Year Published: 2019 Citation: Hinsley, C. A., C. M. Urbanowicz, T. Grout, P. Cappy, S. H. McArt and E. K. Mullen. 2019. 2018 New York State Beekeeper Tech Team Report, 29 pp. https://pollinator.cals.cornell.edu/nys-beekeeper-tech-team/
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Iverson, A. L., C. Hale, L. Richardson, O. Miller and S. H. McArt. 2019. Synergistic effects of three sterol biosynthesis inhibiting fungicides on the toxicity of a pyrethroid and neonicotinoid insecticide to bumble bees. Apidologie 50:733-744. https://doi.org/10.1007/s13592-019-00681-0
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Urbanowicz, C. M., N. Baert, S. E. Bluher, M. Ramos, K. B�r�czky and S. H. McArt. 2019. Low maize pollen collection and low pesticide risk to honey bees in heterogeneous agricultural landscapes. Apidologie 50:379-390. https://doi.org/10.1007/s13592-019-00655-2