Source: UNIV OF MASSACHUSETTS submitted to NRP
INTERACTIVE EFFECTS OF CLIMATE CHANGE AND PATHOGENS ON POLLINATOR HEALTH AND POLLINATION SERVICES: BOMBUS IMPATIENS AND TOMATO
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
COMPLETE
Funding Source
Reporting Frequency
Annual
Accession No.
1029200
Grant No.
2022-67012-38257
Cumulative Award Amt.
$215,826.00
Proposal No.
2021-08382
Multistate No.
(N/A)
Project Start Date
Aug 15, 2022
Project End Date
Aug 14, 2025
Grant Year
2022
Program Code
[A1113]- Pollinator Health: Research and Application
Recipient Organization
UNIV OF MASSACHUSETTS
(N/A)
AMHERST,MA 01003
Performing Department
Biological Science
Non Technical Summary
Pollinator decline is a worldwide concern, and pollinators are threatened by multiple stressorsincluding disease and climate change. Pathogens can be transmitted between pollinators, but we know little about how climate change, including rising temperatures and extreme weather events such as heat waves, will affect pathogen transmission. These two stressors (heat and pathogens) may also interact to impact crop pollination services. My research will address how global warming (heat stress) affects pathogen resistance, transmission, and pollination services, using the common eastern bumblebee, Bombus impatiens, an agriculturally important managed pollinator of tomato and many other crops. Results will be directly relevant to sustainable agriculture by informing best management practices in greenhouse crop production using tomato, and predicting disease spread to manage pollinator health on farms.Many pollinator species have experienced recent range contractions and extinctions linked in part to pathogens. Simultaneously, global agricultural dependence on pollinators continues to increase. Pollinator loss poses a direct risk to human health; pollinator-dependent crops are disproportionately high in macronutrients including Vitamin A and iron, and declines in pollinator abundance raise concerns for food security. Recent work has highlighted the importance of wild pollinators for ecosystem services in agricultural systems and the economic value of pollination ($3251/ha from wild pollinators). Understanding how exposure to environmental stressors impacts pollinator health and ecosystem services has important conservation and economic implications, and is a cornerstone of agricultural climate adaptation.?Temperature and disease are two of the most common selection pressures on insects and the nteractive effects of temperature and immunity have been documented in some insect species, however the effects in native bees are largely unknown. For pollinators, scientists have developed a clearer understanding of the underlying genetic, cellular, and biochemical mechanisms of heat stress, immune response and thermal foraging tolerance of the honey bee, but research on thermal tolerance and interactive effects of temperature and immunity in native pollinators such as bumble bees is in its infancy. Thus, there is a clear need for insights into how climate change affects disease resistance and transmission in bumble bees at multiple scales. Bombus impatiens is the most abundant bumble bee species in the eastern United States and is used for commercial crop pollination. It has the highest mean contribution to crop production, $963 USD/ha, a value more than twice any other non-Apis (honey bee)pollinator in the world.Increasing temperatures are considered a primary factor negatively affecting crop yields. Several globally important crops are sensitive to heat stress during flowering, including many tomato varieties (Solanum lycopersicum L.). Tomatoes grown under elevated temperatures produce fewer pollen grains and less viable pollen. Given that tomato flowers only offer pollen as a pollinator reward, the negative effects of heat stress on pollen production may reduce pollinator attraction directly impacting pollination services.The proposed work is important in understanding how synergistic effects of two major stressors, pathogens and global warming, impact bees and pollination services. Understanding and characterizing responses to physiological and environmental factors is key to making predictions about how organisms will respond to a changing world. I will assess the interactive effects of heat stress and pathogen infection on bee physiology (behavior, resource consumption, and reproduction), pathogen transmission, and pollination services using the gut pathogen (Crithidia bombi) in the native managed pollinator Bombus impatiens. Specifically, in a series of experiments I will use thermal chambers to manipulate the thermal environment of bees and will experimentally infect half of the bees with this pathogen. I will then measure the effects of pollination by infected and uninfected bees to tomato plants to understand the agricultural consequences of infection for tomato production. I will quantify foraging behavior of bees, fruit set, and fruit traits (mass, sugar content, number of seeds) in controlled foraging experiments by infected and uninfected individual bees.Global temperatures have risen 1oC since the Industrial Revolution, and 9 of the last 10 years are the warmest on record (NOAA 2020). Simultaneously, extreme weather events such as heat waves are becoming more frequent, making climate change an urgent and critical component of bumblebee ecology. The proposed research will address critical applied questions on agricultural climate adaptation: the combined impacts of two environmental stressors, global warming and pathogen infection, facing bee populations in the USA. This research will address basic eco-physiological questions about bee health, and measure crop pollination services in a field-realistic, agriculturally important crop that utilizes bumblebee colonies for greenhouse and high tunnel production. Isolating the effects of heat stress on pollinator disease transmission can guide protocols to both optimize agriculturally managed bumblebee health and reduce disease spillover into wild bee populations.
Animal Health Component
50%
Research Effort Categories
Basic
50%
Applied
50%
Developmental
0%
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
21130851070100%
Goals / Objectives
This project seeks to discover how global warming and disease interact to impact bee health and pollination services. More specifically, the major goals of this research are to:Investigate how heat stress affects pathogen resistance and pathogen transmission for the common eastern bumblebee (Bombus impatiens)Assess how heat stress and infection interact to affect pollination services provided by the common eastern bumblebee for growing tomatoes in greenhouses.These research goals are crucial because the common eastern bumblebee is managed for pollinating tomatoes in greenhouses - among other important agricultural applications - and because management practices will benefit from predictions about how these pollinators will respond to interacting stressors in a changing world. To accomplish these goals, this project will investigate the mechanistic connections between individual physiology and community-level behaviors in field-realistic scenarios. The research will measure how the thermal environment and disease interact to impact individual bee health, pathogen transmission within colonies, and pollination services for tomatoes in greenhouses.The objectives of this research assess basic eco-physiological questions about bee health and measurable crop pollination services in field-realistic scenarios for an agriculturally important crop that utilizes bumblebee colonies for pollination in greenhouses.Objective 1. Determine whether infection affects the thermal tolerance of individuals, and whether the thermal environment affects individual pathogen resistance.I will inoculate individual bees with a gut pathogen (Crithidia bombi), subject them to heat stress (thermal environments from 23 C to 40 C in 4 C increments) then measure survivorship and pathogen infection intensity. I will compare these results to measurements from control cases (uninfected bees subjected to the same heat stress treatments).Objective 2. Determine whether the thermal environment affects the rate at which pathogens are transmitted within colonies, and whether the thermal environment affects offspring production for both infected and uninfected colonies.I will introduce one infected individual into replicated microcolonies (9 healthy bees in each microcolony), subject each microcolony to heat stress (thermal environments from 23 C to 40 C in 4 C increments), then (after 14 days) measure pathogen transmission (the percentage of uninfected bees that have acquired infection), and colony reproduction success (brood temperature, egg number, and larval mass). I will compare these results to measurements from control cases (reproductive success for uninfected colonies subjected to the same heat stress treatments).Objective 3. Determine whether pollinator pathogen infection and heat stress (for both plants and pollinators) affect pollination services for tomatoes in greenhouses.I will grow tomatoes in greenhouses controlled to simulate various heat stress scenarios, introduce infected microcolonies to pollinate the tomatoes, then measure fruit set and quality (fruit mass and seed set). I will compare the results to measurements from control cases (tomatoes pollinated by uninfected bees under the same heat stress scenarios).Tomato plants are especially sensitive to heat stress; therefore I will collaborate with my advisory committee (commercial high tunnel tomato growers and University of Massachusetts vegetable crop extension specialists) to identify a realistic range of heat stress scenarios.Understanding the ways that heat stress and disease interact to impact pollination services is important because global change may introduce synergistic interactions between disease dynamics and plant and pollinator health that shape crop yield. This research is critical for climate adaptation. The results of this research will inform best practices for managing disease transmission among pollinators on farms, to advance sustainable crop production (especially for greenhouse tomatoes), and reduce disease spillover into wild bee populations, despite changing environmental stressors.The objectives of this research assess basic eco-physiological questions about bee health, and measurable crop pollination services in a field-realistic, agriculturally important crop that utilizes managed bumblebee colonies for greenhouse and high tunnel production. Isolating the effects of heat stress on pollinator disease transmission can guide protocols to both optimize agriculturally managed bumblebee health and crop production.
Project Methods
General Methods:My research experiments will use female workers of the species Bombus impatiens from commercially sourced colonies and include colony of origin as a random effect in statistical analyses. Workers entering an experiment will be pulled from commercial colonies, assigned to a treatment, and then housed in 500 mL plastic deli cups in an incubator at 27 oC in complete darkness. Bees will be fed 30% sucrose and pollen ad libitum. To infect bees, I will feed each bee 15 µl of inoculum with 9000 Crithidia cells in a 25% sucrose solution. I will make inoculum using locally-sourced Crithidia bombi originally from a wild foraging B. impatiens worker. I will assess infection for all individuals at the end of each trial.To assess infection, I will anesthetize bees with carbon dioxide gas and dissect the intestinal tract into microcentrifuge tubes with 300 μL of Ringer's solution. After waiting four hours to allow the supernatant to settle, I will count Crithidia in a 0.02 μL subsample of a 10 μL aliquot on a hemocytometer with a compound light microscope at 400x magnification. This is a standard protocol for quantifying Crithidia infection intensity, allowing our results to be broadly interpretable.To evaluate pollination services to tomato, I will quantify foraging behavior of bees (floral handling time, intrafloral sonications, flowers visited per foraging bout), fruit set, and fruit traits (mass, sugar content, seeds) in controlled laboratory foraging experiments. I will then compare these metrics between experimentally infected and uninfected worker bumble bees in a flight arena to potted replicate tomato plants.I will extend previous work by testing the thermal tolerance of worker bumblebees under infection stress, as well as the resistance to infection under heat stress; this is very relevant given the high prevalence of this pathogen (up to 80%) in bumblebees in some regions. I will measure the critical thermal maxima in infected and uninfected workers to assess the effects of pathogens on individual thermal tolerance, and will assess how heat stress affects pathogen infection intensity. I will measure critical thermal tolerance following published methods using a controlled temperature ramping rate, with the maximum tolerated temperature (onset of muscle spasms) recorded as the response. I will also measure worker body size for inclusion as a covariate. Statistical models will analyze the effect of infection on thermal tolerance using a hurdle model (presence/absence, followed by infection intensity) and body size as predictor variables, including colony of origin as a random effect.The efforts to enact a change in knowledge through this research will include written and oral communication. I will be providing public facing pollinator talks with local non-profits (Greenfield Trees, Greenfield MA), elementary (Colrain Elementary School, Colrain MA) and middle school groups (Eureka!, Holyoke Middle School, Holyoke, MA), national non-profits - theSierra Club, and the Vassar College Alumni association. The educational talks will focus on pollinator health, the implications for pollinator health in the face of climate change and heat waves, and the measurable actions the public can do to support pollinator health including pollinator plantings, turf replacement, and personal pesticide use reduction.To evaluate the success of this project in collaboration with my advisory committee members, I will create two fact sheets on pollinator health under climate change and pollinator health and pollination services in tomato. These will be disseminated through the advisory committee connections, the UMass Vegetable extension office and NOFA- Pollinator Network. The results of this work will be presented at three professional meetings (Entomological Society of America, AFRI EWD PD and the Sustainable Agricultural Systems NIFA meeting). Information will be further disseminated through my professional connection sites: my personal environmental research and consulting website, and my LinkedIn profile to share project successes, publications and press coverage of my work will be amplified by the University of Massachusetts News Office.

Progress 08/15/23 to 08/14/24

Outputs
Target Audience:During the second year of this project, I reached undergraduate research students at an R1 and primarily undergraduate institution. I worked with a total of 3undergraduate research assistants, and in this time supported 2 undergraduate honors thesis projects. One of these students wont Best Undergraduate Thesis at Mount Holyoke College for our work together. In addition, I communicated with farmers, gardeners and homewoners in Franklin and Hampshire Counties, MA. I gave one public talk on my research in Hadley NY at Hampshire College, and three public talks to homewoners and gardeners who are planting pollinator friendly gardensin Colrain, Heath, and HadleyMA. I worked with the Franklin County Region of Governments to plan regional talks about pollinator conservation, as a part of a state-wide effort to create a pollinator habitat corridor. I had my work highlighted in an exclusive interview and public news article (Mount Holyoke College News) speaking about the effect of heatwaves on bees. Changes/Problems:A major challenge in my work is concerning the Objective 3 project on tomato pollination services. For Objective 3, I engaged fully with this research from March through August 2024 by growing 50 tomato plants from seed in pots. However, a series of repeated failures precluded any meaningful results. I successfully grew the plants to maturation, constructed enclosed flying arenas, and installed a series of bumble bee colonies in these arenas. The concerns, in chronological order were: the plants failed to flower, after ammending the fertilizing regime plants bloomed, and then the local climate hit a heat wave, and all plants aborted these flowers from heat stress, then once the flowers were blooming again, the bees did not visit any flowers after 14 days of close observations. During this time, when no bees were visiting the flowers, the plants began to set fruit, even without insect pollination.Then, those unpollinated fruit all developed blossom end rot. At that point, after 3 months of trials with no meaningul data on the effects of bee pathogen stress on pollination services in crops, I comcluded tomatoes were not going to result in success - and I began to explore other crops as potential replacements for this key objective. I currently have 75 potted strawberries prepared for an April greenhouse experiment, and am exploring blueberry plants as an alternative buzz pollinated, pollinator dependent crop. What opportunities for training and professional development has the project provided?During this reporting period I had a series of mentorship opportunities for professional development. I worked closely with Dr Ike Leslie (UVM) to discuss crop growing strategies in high tunnels, to discuss the tomato concerns I had regarding blossom end rot and failure to flower. I worked closely with my primary mentor Dr Lynn Adler on refining the experimental design, brainstorming alternative solutions when the current plant experiment was not succeeding. I joined a working team in writing a review manuscript with colleagues and mentors at Cornell, UNC, and UMass in co-authoring a review of "MECHANISMS AND CONSEQUENCES OF PLANT-POLLINATOR-PATHOGEN INTERACTIONS" in the Annual Review of Ecology, Evolution, and Systematics. I also attending a series of workshops on regenerative agriculture - No-till farming at Seeds of Solidarity with the American Farmland Trust, as well as planting pollinator habitat with the Franklin County Conservation District. How have the results been disseminated to communities of interest?I have dissemminated my results of the interactive effects of heat stress and pathogens on bumble bee fitness in a series of public and academic talks. I have written and submitted two reearch articles, both currently under review, as well as one review article on bee and plant health. What do you plan to do during the next reporting period to accomplish the goals?I plan to move the remaining funds of my grant to my new institution. I plan to file a "change of project" request to reflect the change in plant (tomatoes to strawberries and blueberries). I plan to resubmit my manuscripts with revisions as soon as they are available.

Impacts
What was accomplished under these goals? During this reporting period I finished all relevant experiments assosiated wtih both objective 1 and 2. I wrote, and submitted for review two manuscripts (not yet accepted, thus not reported in the previous section). This work was successful, and significantly underbudget due to my ability to leverage a series of internal grants and alternative funding pathways to pay undergraduate research assistants.I reported these results at a series of invited talks in New England (Union College, Hampshire College, UMass AMherst, and the MA beekeepers association). I consider this work to be complete, and is now pending acceptance of the two peer reviewed manuscripts. For Objective 3, I engaged fully with this research from March through August 2024 by growing 50 tomato plants from seed in pots. However, a series of repeated failures precluded any meaningful results. I successfully grew the plants to maturation, constructed enclosed flying arenas, and installed a series of bumble bee colonies in these arenas. The concerns, in chronological order were: the plants failed to flower, after ammending the fertilizing regime plants bloomed, and then the local climate hit a heat wave, and all plants aborted these flowers from heat stress, then once the flowers were blooming again, the bees did not visit any flowers after 14 days of close observations. During this time, when no bees were visiting the flowers, the plants began to set fruit, even without insect pollination.Then, those unpollinated fruit all developed blossom end rot. At that point, after 3 months of trials with no meaningul data on the effects of bee pathogen stress on pollination services in crops, I comcluded tomatoes were not going to result in success - and I began to explore other crops as potential replacements for this key objective. I currently have 75 potted strawberries prepared for an April greenhouse experiment, and am exploring blueberry plants as a different buzz pollinated pollination dependent crop. At the end of this reporting period, until present, I have transitioned from postdoctoral fellow to an Assistant Professor of Ecology and Global Change at Hampshire college.The transition of the funds (and pause in availability of said funds) from UMass to Hampshire have significantly delayed a continuation of progress on Objective 3.

Publications


    Progress 08/15/22 to 08/14/23

    Outputs
    Target Audience:During the first year of this project, I reached undergraduate research students at an R1 and private university. I worked with a total of 8 undergraduate research assistants, and in this time supported 2 undergraduate honors thesis projects. In addition, I communicated with farmers in Franklin County, MA. I gave one public talk on my research in Schenectady NY, and one public talk to small-scale farmers about farming with pollinators in Colrain MA.I have worked with the Franklin County Region of Governments to give regional talks about pollinator conservation, as a part of a state-wide effort to create a pollinator habitat corridor. Changes/Problems:In Specific Aim 2 I planned to look at pathogen transmission rates. I executed this project, with high sample size in late 2022. However, I had extremely low rates of transmission - too low to confidently conclude anything (less than 2%, I was anticipating 20-60%). Because of this, I shifted specific aim 2 to address colony reproductive output, colony behavior under stress, and addedtwo new projects in 2023 to look at how individual bee thermal regulation and oxygen respiration rate is impacted by heat and pathogen stress. These projects were a success, results are compelling, and the manuscript is in preparation now. I am concerned that my original plan for Specific Aim 3- to apply thermal stress to the tomato plants will be problematic, after extensive discussions with local growers and UMass tomato experts. To address this ahead of time, I will be first looking at just pathogen stress alone on bees and the resultant tomato fruit set. Then running the heat stress experiment, so that I can be confident to have results from this project (and not just aborted tomato fruits on all plants, which is what growers predict). What opportunities for training and professional development has the project provided?I have trained 11 undergraduate research assistants. One of which has gone on to apply for veterinary school, specifically with hands-on animal/insect husbandry skills appropriate for the new veterinary guidelines for bees. As the postdoctoral research fellow on this grant, I have attended professional development seminars at UMass Amherst, taught a new course on Field Ecology in the Biology Department at UMass Amherst. I have collaborated widely with non-biology scientists to learn new techniques on technology including the use and development of Arduino based monitors, audio recording analysis, and biochemical ecophysiological analysis of bees. How have the results been disseminated to communities of interest?Yes, I have been speaking with tomato growers directly, but results that are specifically pertinent to tomatoes will not be available until year two. What do you plan to do during the next reporting period to accomplish the goals?I will grow tomatoes in a greenhouse, run the experiments on bee visitations. I will hire 2 research assistants from the pool of students I have already trained.

    Impacts
    What was accomplished under these goals? I have successfully accomplished the research goals of Specific Aim 1 and 2. My results were highlighted in the quad chart shared with the NIFA remote conference in September.I have two unique publications in preparation for submission right now, and am finished collecting all data relevant to them. The results are exciting, and I look forward to publishing them! This leaves only specific Aim 3 for the second year, as planned. I am on track to accomplish all the research goals set out in this grant.

    Publications