Source: BOWLING GREEN STATE UNIVERSITY submitted to
WHERE IS POLLINATION IN PERIL? EVALUATING CLIMATE RISKS TO WILD AND MANAGED BEES AND POLLINATION SERVICES ACROSS THE US
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
NEW
Funding Source
Reporting Frequency
Annual
Accession No.
1023404
Grant No.
2020-67013-31916
Project No.
OHOW-2019-06138
Proposal No.
2019-06138
Multistate No.
(N/A)
Program Code
A1113
Project Start Date
Aug 1, 2020
Project End Date
Jul 31, 2024
Grant Year
2020
Project Director
McCluney, K.
Recipient Organization
BOWLING GREEN STATE UNIVERSITY
319 ADMINISTRATION BLDG
BOWLING GREEN,OH 434030001
Performing Department
Biological Sciences
Non Technical Summary
This project seeks to understand where pollinators and pollination services are most at risk from climatic variability. We will accomplish this goal by linking physiological responses to climate, to pollinator health and pollination across 100 sites in 10 US cities that cover 6 states and 12 USDA climate zones. In each background climate, urbanization itself creates microclimates that vary in temperature and moisture, allowing assessment of pollinator performance under a wide range of climate conditions both in and outside of cities. Working with several common taxa, our objectives are to: 1) assess bee vulnerability to warming and drought across a range of taxa and background climates, 2) document consequences of warming and drought for pollinator health and abundance, and 3) link changes in pollinator physiology, health, and abundance to pollination services. These objectives will be accomplished by: 1) measuring physiological tolerance to warming and dehydration, as well as body temperatures and water contents of foraging bees, 2) measuring pollinator health (lipid and glycogen stores) and abundance, and 3) measuring pollen deposition in a model crop. Combined, these approaches will identify which pollinator species are most at risk of heat and drought stress, and which regions of the US could suffer greatest climate-related loss of pollinators and pollination service. These results would provide the first mechanistic assessment of how temperature and water balance influence bee health, population sizes, and pollination services across the US. Thus, the described research will address this RFA by helping understand risks to pollinator health.
Animal Health Component
100%
Research Effort Categories
Basic
50%
Applied
50%
Developmental
(N/A)
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
3063085107090%
3063010107010%
Goals / Objectives
The long-term goal of the proposed research is to assess risks posed to pollinators and pollination, by variation in temperature and moisture, across the US. This work will support development of management strategies to mitigate climate-driven loss of agricultural pollination services, including in urbanized areas. We have three specific objectives:1) Assess bee vulnerability to warming and drought across a range of taxa and background climates ("Sensitivity and Exposure"). For multiple species, we will measure both sensitivity (physiological limits) and exposure (body temperatures and hydration states of foraging bees) to warming and drought. Results will indicate the relative risks posed to bee communities by temperature versus hydration, and will distinguish among competing hypotheses about key predictors of sensitivity and risk--including background climate, local microclimate, life history traits, and adaptation.2) Document consequences of warming and drought for pollinator health and abundance ("Health and Abundance"). We will measure health (energetic state) and abundance of pollinator taxa, across sites that vary in urban warming in each city. We predict that, in the hottest or driest urban sites, the most vulnerable species identified in Objective 1 will also experience reduced health and abundance.3) Link changes in pollinator physiology, health, and abundance to pollination services ("Pollination"). We will measure visitation rates and pollen deposition per visit per species for a common and important model garden plant. We will then link these observations to pollinator physiological state and environmental conditions, developing predictive models for how climatic variation will influence pollination service.Across these three objectives, we will also record and examine potential site covariates already known to modulate bee abundance and diversity in other studies, such as floral resources and shade. These covariates will be important to statistically account for uncontrollable variation between sites, and will also provide clues to potential management solutions to better buffer pollinators and pollination against the effects of climate change.
Project Methods
To accomplish our goals we will link physiological responses to climate and to pollinator health and pollination across 100 sites in 10 US cities that cover 6 states and 12 USDA climate zones. Here we briefly summarize our methods. More details can be found in the full proposal.First, to assess bee vulnerability to warming and drought we will assess sensitivity, exposure, and adaptability. We will measure the physiological limits of each bee species by calculating thermal maximum and dehydration tolerance. We will then measure their field body temperature and water content, calculating their safety margins (proximity to physiological limits). These measures will be collected for multiple bee taxa (> 6) across a gradient of temperature and moisture in each of 10 cities, and over time, relating climate to physiological condition. Examining changes in physiological limits across these gradients of temperature and moisture allows us to assess adaptability of each species to each condition.Second, we will link changes in climate and bee physiology to bee health and abundance by measuring energy reserves of each bee and the abundance of each species of bees at each location. Then we will relate these metrics of health and abundance to the previously calculated safety margins.Third, we will link our previous measurements to changes in pollination services by measuring bee visitation rates, visitor species composition, and per visit pollination efficiency for a model plant species, cucumber. We will then relate visitation rates to measures of safety margins and aggregate pollination services to our measures of climatic conditions.Across all objectives, we will measure important potential covariates (e.g. shade) to statistically control for their potential influence and help develop management recommendations. For each objective we will evaluate success based on the numbers of peer-reviewed and non-technical publications, presentations to both academic and non-technical audiences, and stakeholders reached. These efforts will disseminate new knowledge of how changes in urbanization and climate influence bees and pollination, with potential implications for management and for future research.

Progress 08/01/22 to 07/31/23

Outputs
Target Audience:During the project period we reached members of the scientific community through department seminars and scientific conferences, undergradaute and graduate students involved in the project, urban gardeners, farmers, and beekeepers through interactions preceeding, during, and after research, and the general public through non-scientific presentations and events. Changes/Problems:This year we sampled similarly to the previous year without many large changes, except that we focused on filling gaps in previous data collection. Additionally, we realized that the window for cucumber flowering in AZ was a narrow period in May with high daytime temperatures (>105 °F) that allowed us to accomplish multiple goals simultaneously with a single sampling. Thus we decided to sample AZ only once in summer 2023 instead of twice like the previous year. This also conserved dwindling travel funds, which were no longer adequate for originally planned sampling, due to inflation. Unfortunately, we continued to have challenges keeping our cucumber alive and in good condition within pots in AZ, despite substantial effort (watering multiple times per day). More shade was likely needed, but this was not readily available at the places we stayed during our travel. This limited our pollination data in AZ. In the previous annual report we also mentioned that we had experienced difficulty in measuring the desiccation limits of honey bees. Unfortunately, we were not able to come up with a solution for this, despite attempts, and thus stopped measuring their desiccation limits in summer 2023. However, it is possible that we will still be able to use the data we collected from summer 2022 in some way. In particular, although control honey bees with water did not live longer than desiccation trial bees, the 10th percentile of final water content for desiccation trial bees may still provide some indication of tolerance (i.e. even if some honey bees died prematurely from something unrelated to desiccation, the bees that survived the longest likely did die do to desiccation rather than other causes). What opportunities for training and professional development has the project provided?As the project has developed, previous team members with more experience have trained new team members, helping them learn or improve skills with bee identification and collection maintenance, geographic information systems, environmental physiology, vegetative surveying, cucumber cultivation, best practices in data management, and project management. This included training for 12 undergraduate and 5 graduate students and 3 faculty. Training occurred through virtual video meetings as well as in-person, hands-on activities. One of the graduate students received his MS and started a position with the USGS Native Bee Inventory and Monitoring Lab in Maryland. How have the results been disseminated to communities of interest?During the project period, we prepared summary sheets for each garden that gave them information about the top 5 bee taxa found in their garden and highlighted flowers that were heavily visited by bees across their city. We also shared results from related graduate student projects with the scientific community via conferences (results from the overall project began to be shared in the next project period). Finally, we continued to share observations on social media. What do you plan to do during the next reporting period to accomplish the goals?In the next project period, we will focus heavily on processing samples collected during the previous project periods, especially measurements of bee hydration, identification of bees to the species level, measures of pollination efficiency, and measures of energy reserves of selected individuals. We will also greatly increase our data analysis efforts, developing publications that will communicate our results to the scientific community. As results are finalized, we will also work to communicate these results to participating gardens/farms, and the general public.

Impacts
What was accomplished under these goals? During the project period we obtained additional data for bee field body temperatures and water content & limits (specific objective #1), bee abundance (specific objective #2), and pollination of cucumbers (specific objective #3) in all 10 cities. Field data collection continued from the previous project period into August 2022 and then began again in May 2023, continuing through the end of the project period in July 2023. Laboratory data collection occurred throughout the project period. Research was conducted at 4-8 urban gardens/farms in each of the 10 cities (Detroit, Toledo, Raleigh, Durham, Atlanta, Augusta, Denver, Fort Collins, Phoenix, Tucson), with a total of 12 urban gardens/farms sampled within each region. Surveys were conducted twice in cities in GA and NC (cities where the period of cucumber flowering does not coincide with hot, potentially stressful conditions for bees) and once for cities in AZ, CO, and MI/OH (cities where the period of cucumber flowering does coincide with hot, potentially stressful conditions for bees). Extra effort was put into filling in gaps in data from previous sampling efforts. Sample processing and data entry is ongoing, but we have conducted preliminary analyses of physiological limits, field body temperatures and water contents, and safety margins. There are several interesting preliminary findings: Taxa differ considerably in their median thermal (42-50 °C) and water content (48-63%) limits across all locations There appears to be little correlation between thermal and water content limits. Being thermally tolerant appears to be unrelated to being desiccation tolerant. Approximately two thirds of taxa tend to be more dehydrated when their body temperatures are higher Approximately half of taxa are sometimes near their thermal limits in AZ cities. This finding should be viewed as tentative as we are currently using estimates of limits that do not vary by location. Bumble bees are often near their thermal limits in GA, NC, and CO cities (rarely found in AZ cities). This finding should be viewed as tentative as we are currently using estimates of limits that do not vary by location. Smaller bee taxa appear to have higher water content safety margins, on average, while larger bees often have narrow margins. This finding makes sense given that smaller bees have higher surface area to body mass ratios that promote rapid desiccation (our desiccation time data also shows that some of these smaller taxa have short desiccation times). Thus, it would be more important for these bees to have larger buffers when desiccating conditions occur. Many bee taxa have some individuals near their water content limits at some point in time, across many locations. However, more data are needed to assess differences between locations. These patterns are based on preliminary analyses of incomplete data and should be taken with caution until more complete analyses are possible. Data collected for this project has also supported tangentially-related analyses by students associated with the project, including: MS student Francis Mullan completed his thesis on the effects of warming on bumble bee health. Undergraduate Malia Naumchik published her research showing the bumble bee body temperatures increase with greater pollen load and that this increase could cause some individuals to near their thermal limits. MS student Bridget Harter analyzed how urban landscapes influenced the diversity of bees in Raleigh, NC for her thesis. She found that the amount of greenspace edge in the area surrounding the site was positively associated with bee diversity. Additionally, including estimates of accessibility of these greenspace edges (accounting for barriers to dispersal) strengthened the relationships.

Publications

  • Type: Journal Articles Status: Published Year Published: 2023 Citation: Naumchik, M., & Youngsteadt, E. (2023). Larger pollen loads increase risk of heat stress in foraging bumblebees. Biology Letters, 19(5), 20220581. https://doi.org/10.1098/rsbl.2022.0581
  • Type: Theses/Dissertations Status: Published Year Published: 2022 Citation: Mullan, F. (2022). Connecting above-and belowground effects of climate warming on bumble bee health.


Progress 08/01/21 to 07/31/22

Outputs
Target Audience:During the project period we reached members of the scientific community through department seminars and scientific conferences, undergradaute and graduate students involved in the project, urban gardeners, farmers, and beekeepers through interactions preceeding,during, and after research, and the general public through non-scientific presentations and events. Changes/Problems:One challenge has been measuring the water content limits of honey bees (especially) and bumble bees (to a lesser extent and for certain species), as well as a few rare taxa, due to poor survival in the lab for the duration needed for desiccation tests. We are working to develop new methods that may increase survival (e.g. housing honey bees in groups in desiccation containers). However, if these new methods are not effective, for these taxa we may be unable to calculate robust estimates of water content limits, and thus also water content safety margins. We would still be able to calculate thermal limits and thermal safety margins and could still measure field water content and examine deviation from optimal water content. We have also modified our schedules of activities for each task to improve tractability, while still achieving project goals. For example, our original planned schedule had us collecting from multiple sites per day, during key periods of observation, on multiple days per sampling event. But we found that this was not practical, having challenges both in terms of logistics (causing excessively long sampling events and lots of driving), and in terms of project goals (time of day has larger effects that originally anticipated, making sampling at consistent times of day important; long holding times for bees collected in the field reduces survival, thus bees need to be returned to the lab for limits measurement quickly). Thus, we are now only sampling one site per day, per team, allowing us to be present during important observation windows and to promptly return bees to the lab for testing of physiological limits. The total sampling effort is similar to our originally planned schedule, just distributed over fewer days, and we don't lose time to excessive travel What opportunities for training and professional development has the project provided?As the project has developed, previous team members with more experience have trained new team members, helping them learn or improve skills with bee identification and collection maintenance, geographic information systems, environmental physiology, vegetative surveying, cucumber cultivation, best practices in data management, and project management. This included training for 10 undergraduate and 4 graduate students, two research technicians, and 3 faculty. Training occurred through virtual video meetings as well as in-person, hands-on activities.Multiple undergraduates/techs subsequently began graduate programs. One of the graduate students received his MS and started a position with the USGS Native Bee Inventory and Monitoring Lab in Maryland. How have the results been disseminated to communities of interest?Although we currently have limited results to report, we have provided gardens/farms with lists of bee taxa found at their locations (along with our bee identification guide). We have also shared results from related graduate student projects with the scientific community via conferences. These projects included partial data from the larger project. Finally, we continued to share observations on Twitter (example). What do you plan to do during the next reporting period to accomplish the goals?In the next project period, we will process samples collected during the previous project period, allowing us to calculate thermal and water content safety margins for bees in all cities. We will also begin determining the energy reserves of selected individuals, to examine how safety margins influence bee health. We will also begin our 3rd season of sampling, adding to previous data on bee body temperatures and water contents, temperature and water content limits, safety margins, bee health, bee abundance, and pollination in all 10 cities. We will also expand on our preliminary data analyses, beginning to develop publications that will communicate our results to the scientific community. As results are finalized, we will also work to communicate these results to participating gardens/farms, and the general public.

Impacts
What was accomplished under these goals? During the project period we expanded our measurements of bee body temperatures and water content (specific objective #1), bee abundance (specific objective #2), and pollination of cucumbers (specific objective #3) to 5 additional cities and continued to add to existing data in the 5 previously sampled cities. We also began measuring critical thermal limits and critical water content limits for bees (specific objective #1) from all sites and cities. This involved developing methods that were more portable and scalable than anything previously attempted for bees. Field data collection continued from the previous project period into August 2021 and then began again in May 2022, continuing through the end of the project period in July 2022. Laboratory data collection occurred throughout the project period. Research was conducted at 4-8 urban gardens/farms in each of the 10 cities (Detroit, Toledo, Raleigh, Durham, Atlanta, Augusta, Denver, Fort Collins, Phoenix, Tucson), with a total of 12 urban gardens/farms sampled within each region. Surveys were conducted twice in cities in GA, NC, and AZ (southern cities where the period of cucumber flowering does not coincide with the hottest, most stressful conditions for bees) and once for cities in CO and MI/OH (northern cities where the period of cucumber flowering does coincide with the hottest, most stressful conditions for bees). Extra time was spent sampling Phoenix, AZ, making up for the lack of sampling at that location in May 2021, when we were unable to sample due to COVID-19 restrictions. Sample processing and data entry is ongoing, but we conducted limited preliminary analyses. One initial interesting observation is that multiple taxa of bees seem to have relatively invariable body water content if collected when they have lower body temperatures (often in the morning), but variation in body water content increases substantially at higher body temperatures, which may indicate that some bees are dehydrated at these hotter temperatures. The extent to which this occurs appears to vary between species. However, these patterns are based on preliminary analyses of incomplete data and should be taken with caution until more complete analyses are possible. Data collected for this project has also supported tangentially-related analyses by students associated with the project, including: While working as an undergraduate tech on the project, Malia Naumchik chose to pursue a complementary independent project asking whether bumble bees with larger pollen loads had hotter body temperatures. She compared her measured body temperatures to CTmax data collected as part of this project to show that large bees on hot days would be at risk of lethal body temperatures if they collected full pollen loads. She presented her results at an undergraduate research symposium in fall 2021 and has a manuscript in prep for submission to Biology Letters in fall 2022. As a USDA REEU student in the BeeMORE program, Peyton Rudman assisted with this project and collected additional data during single-visit pollination observations for this project to ask whether honey bees and bumble bees were more effective pollinators when they stayed for longer visits on cucumber flowers. She presented her results at an undergraduate research symposium in summer 2022. While working as a Masters student on the project, Francis Mullan completed his thesis on how temperature impacts bumble bees inside and outside of their nest. He measured nest temperature throughout the 2021-2022 growing season and conducted lab experiments on bumble bee thermoregulatory behaviors. He combined data from these projects with our measurements of field body temperature and visitation rates to develop a comprehensive model of the direct effects of temperature on bumble bee performance. Francis successfully defended his thesis in summer 2022 and has a manuscript in preparation.

Publications


    Progress 08/01/20 to 07/31/21

    Outputs
    Target Audience:During the project period we reached members of the scientific community through department seminars and scientific conferences, undergradaute and graduate students involved in the project, urban gardeners, farmers, and beekeepersthrough interactions preceeding and during research, and the general public through non-scientific presentations. Changes/Problems:The main change to the project is that we are now only conducting one sampling event in northern cities per year because the timing of cucumber flowering coincided with the hottest period of the summer in those cities. Making this change has improved the manageability of the summer schedule. We also are now planning to sample 12 sites across each pair of cities in years 2 and 3, which may be divided as 6 in each city or might be 8 sites in the larger cities and 4 sites in the smaller cities, depending on site availability in the smaller cities. This change was needed in order to have time to sample all cities over the course of the summer with necessary breaks for project personnel. We note that ongoing pandemic restrictions and vaccine timing prevented us from conducting our first sampling trip in Phoenix, AZ in the spring of 2021, but we will complete that work in the spring of the next project period, along with planned 2022 work, in a longer sampling trip. What opportunities for training and professional development has the project provided?Members of the team worked together to improve our skills in multiple areas, including bee identification, geographic information systems, environmental physiology, vegetative surveying, cucumber cultivation, and best practices in data management. This included training for 4 undergraduate and 3 graduate students, a research technician, and 3 faculty. Training occurred through virtual video meetings as well as in-person, hands-on activities. How have the results been disseminated to communities of interest?Results are limited at this time. However, we have communicated some observations with the scientific community and the general public on Twitter. Additionally, graduate student Francis Mullan presented at the Southeastern branch meeting of the Entomological Society of America (virtual) on this and related work on the responses of bumble bee colonies to warming. Moreover, the Atlanta Botanical Garden press department shared our discovery of an endangered bee living in downtown Atlanta, Bombus fraternus, through their social media department. Finally, our research project has also been featured in BGSU News and Kennesaw State Magazine. What do you plan to do during the next reporting period to accomplish the goals?In the next project period we will process the samples and analyze the data previously collected in order to understand daily variation in bee physiology, activity, and pollination. We will then use this information to allow us to expand our measurements, and include more sites in all 10 cities (5 pairs of cities). New measurements will include temperature and water content limits for bees, as well as key metrics of bee health related to energy stores. We will simultaneously continue measuring bee body temperatures and water content in the field, abundance, certain pollination metrics, and habitat characteristics, allowing us to more fully connect environmental conditions to bee physiology, health, abundance, and pollination. We will also present our results at seminars, conferences, and meetings, and provide reports to local partners and site managers.

    Impacts
    What was accomplished under these goals? During the project period, we developed, refined, and implemented protocols to measure bee body temperatures and water content (specific objective #1), refined an approach for measuring bee abundance (specific objective #2), and measured pollination of cucumbers (specific objective #3). All of this work focused on making frequent observations from dawn until mid-afternoon in order to understand how these measurements vary throughout the day and to relate weather and habitat to physiology, activity, and pollination. Data collection began in May 2021 and continued beyond the project period end date. This work was conducted at 8 urban gardens/farms in each of 5 cities (Detroit, Raleigh, Atlanta, Denver, Phoenix), with surveys conducted twice in Atlanta and Raleigh (southern cities where the period of cucumber flowering does not coincide with the hottest, most stressful conditions for bees) and once for Denver and Detroit (northern cities where the period of cucumber flowering does coincide with the hottest, most stressful conditions for bees). In the southern cities, sampling during the hottest period was focused on bees and did not include pollination due to the lack of flowering cucumbers, while sampling during peak cucumber flowering involved all activities. Phoenix sampling occurred only once in this project period due to pandemic restrictions during the early period of cucumber flowering in that location preventing travel, but the necessary work will be conducted in that location during the next project period instead. Data analysis had not yet begun by the end of this project period, because data was still being collected, so results are not yet available to report. However, anecdotally, we observed bee activity decline above a certain temperature in Phoenix, AZ (not yet quantified), but also measured a single bee with a body temperature of ~48 degrees celsius (119 degrees fahrenheit), which is tied for the hottest body temperature measured in bees.

    Publications