A systems approach to understanding the impacts of sublethal doses of neonicotinoids on bumblebee and honeybees

Lead Research Organisation: University of Exeter
Department Name: Biosciences

Abstract

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Technical Summary

Neonicotinoid insecticides are used to protect a range of crops such as oilseed rape and cereals against herbivores. They are also used as foliar sprays on soft fruit crops and are widely sold for garden use on flowers, fruit and vegetable crops. Evidence is mounting that exposure of bees to neonicotinoids produces sublethal effects such as reduced navigational ability that are not detected in laboratory assays or in field trials where hives are adjacent to a treated flowering crop.

This project will quantify the levels of neonicotinoids found in crops and wildflowers in UK arable farmland, and feed these into landscape maps of the distribution of floral resources (produced in a parallel project, BB/J014753/1, starting 2013). We will quantify the doses of neonicotinoids that honeybee and bumblebee colonies are naturally exposed to, before going on to assess the impacts of this exposure on bumblebee colony performance. Exposure and impacts will be examined by both empirical studies and modelling approaches. An existing integrative model of a honeybee colony development, which predicts forager behaviour and colony performance, is being adapted for bumblebees in project BB/J014753/1. These models will enable us to predict where both honeybee and bumblebee workers will forage, and thus predict their exposure, which will be compared to that recieved by real nests placed in the landscape. We will then examine whether exposure to neonicotinoids at realistic field levels alters or impairs foraging behaviour using Rothamsted's unique harmonic radar facility. These data will be used to develop a sub-model for both honeybees and bumblebees which includes impacts of neonicotinoids in predictions of colony success, which will be tested with real colonies of bumblebees in field experiments. We will use the model simulatons to develop management recommendations to minimise the impacts of neonicotinoids on both managed honeybees and wild bumblebee populations.

Planned Impact

The impact of this project will be a substantially enhanced understanding of the role of sublethal exposure to neonicotinoids on the predominant pollinator groups, honeybees andbumblebees, in arable farmland; and a modelling tool to help in the risk assessment process. The project has clear relevance for understanding how pest management decisions impact on the provision of a vital ecosystem service (pollination). It aims to produce management recommendations which will mitigate negative effects and ultimately help to enable us to farm sustainably. It is therefore of high relevance to many stakeholders. Pollination is crucial for farmers, and our results will help ensure that bees can be deployed practically and sustainably to provide good yields for appropriate crops. This will become increasingly important as summers become warmer and drier and new crop species are planted e.g. sunflower, which depend on insect pollination but are generally treated with neonicotinoids.

Who will benefit and how?

Policy makers (e.g. Defra)
The project will provide large new datasets, and an interactive web-based tool modelling bee colony development, to aid policy makers and regulators in regional, national, EU and other agencies. These will serve as the basis for the development of sound policies with respect to pesticide use and pollination, as well as practical advice and recommendations to practitioners in the land-based industries.

Farmers, beekeepers and the agri-food industry
Our data will provide much-needed information on the safety of this class of agrochemical for both managed and wild bee populations, and will provide practical advice on how best to balance the clear conflict between pest control and pollination. This is particularly acute in soft-fruit farming where farmers currently buy bumblebee nests while using systemic insecticides. The lead PI has previously given talks to soft fruit growers at the James Hutton Institute at their annual event where growers are invited to meet and talk to researchers, and this approach will be used again. Similarly, the lead PI has spoken at the annual British Beekeepers Association conference, and writes a regular column for their newsletter, and both methods will be used to convey the results of this project to the beekeeping community. Three large agrochemical companies have actively been requesting the development of a model to predict exposure to neonicotinoids and subsequent effects at the colony level so this project provides an opportunity to contribute to this, independently, with the results being directly useful to the industries.

The NGO community: wildlife, conservation and environmental organisations and advisors.
Conservation organisations and stakeholders, such as Natural England, British Trust for Ornithology, the RSPB, The Game and Wildlife Conservation Trust, Butterfly Conservation, Bumblebee Conservation Trust and the British Beekeepers Association already collaborate with us and utilise the results we publish to enhance public awareness and advise land managers.

The public
The public at large are fascinated by bees and pollination, and rely on them for production of food to ensure a healthy and balanced diet. The applicants have excellent track records in reaching a wide audience with high profile and exciting science, via talks, specific events (workshops, Open Days, Hampton Court Flower show exhibits etc) and all forms of media (web, press, radio, television). We will continue to use all these types of communication to maximise impact. Enhancing public awareness and understanding of such issues is likely to play a key role in influencing policy makers to adopt appropriate changes.
 
Description We performed field experiments to assess whether bee navigation and foraging behaviour are affected by sub-lethal levels of neonicotinoid pesticide in nectar. The resuts were mixed suggesting some slight effects of very low doses of neonicotinoid both on navigation behaviour, and on foraging choices in relation to sugar concentration.

We have developed a module for incorporation into the honeybee model BEEHAVE. This module simulates the applications of various pesticides at any food source in the landscape, their influx via contaminated nectar and pollen into the colony and, based on dose response relations, lethal and sublethal effects on exposed bees (e.g. increased mortality rates, changes in foraging and recruitment behaviour). Simulating the effects of increased mortality of different life stages on colony survival, demonstrated that the colony is most vulnerable to increased mortality of in-hive workers (nurse bees), compared to losses of brood or foragers (Rumkee et al, 2015). The strongest effects occur when colonies are exposed in Spring (Rumkee et al, 2015). We also modelled the effects of non-random food storage by bees in the combs of the hive. Simulations showed how the behaviour of receiver bees in receiving nectar, placing it in the comb, and feeding it to larvae, can affect the level of pesticide residues that enter the brood (Rumkee et al, 2017).
Exploitation Route The incorporation of the potential effects of pesticides into our honeybee and bumblebee models will enable them to be used in pesticide risk assessment by regulators, policy makers and industry, simulating pesticide exposure landscapes and predicting the responses of bee colonies to pesticides when individuals are exposed. This will be of value to all those interested in crop production, bee conservation or conservation of wild flower communities.
Sectors Agriculture, Food and Drink,Environment

 
Description The incorporation of the potential effects of pesticides into our honeybee and bumblebee models will enable them to be used in pesticide risk assessment by regulators, policy makers and industry, simulating pesticide exposure landscapes and predicting the responses of bee colonies to pesticides when individuals are exposed. This will be of value to all those interested in crop production, bee conservation or conservation of wild flower communities. We were also awarded the BBSRC Innovator of the Year Award for Social Impact in 2017 for our work using bee models to support decision making by policy makers, regulators and farmers. Since the grant finished Bayer, Syngenta and BASF have been evaluating the models further to support their risk assessment trials for pesticides and ensure their field trials are designed to capture effects at the colony scale over appropriate time periods (Agatz et al, 2019, Environmental Toxicology & Chemistry). In 2020 EFSA advised member states that it would be appropriate to use the BEEHAVE and Bumblebeehave models to set new bee health protection goals for EU risk assessment. IN 2021 EFSA published a report demonstrating the use of BEEHAVE for this purpose in terms of assessing colony size variability.
Sector Agriculture, Food and Drink,Environment
Impact Types Societal

 
Description Citation in EFSA publication on importance of BEEHAVE model in building regulatory framework on multiple stressors for bees
Geographic Reach Europe 
Policy Influence Type Citation in other policy documents
Impact Improving the regulatory environment for pesticides and other environmental stressors by incorporating a systems modelling approach. BEEHAVE is being used as the basis of the EFSA conceptual model
URL http://ac.els-cdn.com/S0048969716320587/1-s2.0-S0048969716320587-main.pdf?_tid=18c0f7dc-04b0-11e7-af...
 
Description EFSA Report: Evaluation of BEEHAVE model for use in assessing the effects of multiple stressors, including pesticides, on bees
Geographic Reach Europe 
Policy Influence Type Citation in systematic reviews
URL http://www.efsa.europa.eu/en/efsajournal/pub/4125
 
Description EFSA report: Used to demonstrate use of BEEHAVE to risk managers to assess honeybee colony size
Geographic Reach Europe 
Policy Influence Type Implementation circular/rapid advice/letter to e.g. Ministry of Health
URL https://efsa.onlinelibrary.wiley.com/doi/epdf/10.2903/sp.efsa.2021.EN-6518
 
Description Implementing National Pollinator Strategy Workshop: Silwood Park March 2015
Geographic Reach National 
Policy Influence Type Influenced training of practitioners or researchers
 
Description Invited Experts EFSA Workshop on assessing BEEHAVE as a tool for risk assessment
Geographic Reach Europe 
Policy Influence Type Citation in other policy documents
 
Description Recommended use by EFSA of BEEHAVE models to set new bee protection goals for risk assessment
Geographic Reach Europe 
Policy Influence Type Citation in other policy documents
Impact The European Food Standards Agency (EFSA) oversees the regulation and risk assessment of agrochemicals in the EU. In May 2020 EFSA reviewed its Guidance Document for assessing risks of chemicals to bees, which sets the Specific Protection Goals for bees defining the magnitude of effect (e.g. on colony survival) that would be 'safe' for field trials. EFSA proposed four 'approaches' to setting new Specific Protection Goals to the EU risk managers in member states, and two of these involved using BEEHAVE & Bumble-BEEHAVE. In August 2020 the European Commission confirmed in a written Question & Answer to the European Parliament that "A majority of Member States supported to conduct further work based on approach 2, which considers natural variability in colony size. It is based on scientific population modelling, in particular the BEEHAVE model, which EFSA found in 2015 to predict well colony dynamics."
 
Description BEEHAVE validation meeting UFZ 2019 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Industry/Business
Results and Impact A meeting of BEEHAVE users from industry (Bayer, Syngenta, BASF) and academia to discuss the validation of the model with existing data set and future changes to the model.
Year(s) Of Engagement Activity 2019
 
Description EURBEE 2014: Modelling the impacts of various pesticide effects on the honeybee colony 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Type Of Presentation poster presentation
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Poster presented in the 'effects of stressors on the behaviour of bee pollinators' section, Eurbee 6, Murcia, Spain

invitations to work with others using BEEHAVE
Year(s) Of Engagement Activity 2014
 
Description Hands-on demonstration to joint Cornwall & West Cornwall Beekeepers' convention (BOAD) 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Professional Practitioners
Results and Impact A hands-on demonstration & stand introducing the BeeHave model to explore the impact of multiple stressors on honeybee colony development & survival. Encouraging direct participation and exploration of the model at the joint Cornwall & West Cornwall Beekeepers convention (BOAD 2014) and equipping the audience to utilise the model at their leisure.
Year(s) Of Engagement Activity 2014
 
Description Host: South West Bee Disease and Husbandry Day May15 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? Yes
Geographic Reach Regional
Primary Audience Professional Practitioners
Results and Impact Busy and full day of training sessions, workshops and talks delivered by Bee Inspectors. My Research Team showed posters and hosted the event, explaining research from various projects to 65 beekeepers

Much better awareness of our research group at the ESI, Penryn. And our research team have better knowledge of regional beekeepers
Year(s) Of Engagement Activity 2015
 
Description ITV programme: The Queen's Garden - TV appearance looking at bee foraging patterns 
Form Of Engagement Activity A press release, press conference or response to a media enquiry/interview
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Interest from general public in how we research where bees go.

*
Year(s) Of Engagement Activity 2015
 
Description Invited talk at the Cornwall Beekeepers Association AGM on current bee research within our group. 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Professional Practitioners
Results and Impact Presented a talk to the Cornwall Beekeeping Association on "Bee research on the Penryn campus" introducing the diversity of projects currently engaged in and stimulating discussion of the bee models developed & under development, multiple factors affecting bee survival & development in a changing & patchy landscape, and current concern about pesticides.
Year(s) Of Engagement Activity 2015
 
Description RIFCON modelling workshop 2019 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Industry/Business
Results and Impact I had a three hours slot on a two days workshop on mechanistic effect modelling at the consulting company RIFCON (Germany) for a presentation and exercises on our bee models. There were 8 participants and ca. 6 employees involved.
Year(s) Of Engagement Activity 2019
URL https://www.rifcon.de/en/workshop
 
Description Royal Cornwall Show 8th-10th June 2017, University of Exeter Stand 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact We were part of a public engagement stand at the Royal Cornwall show where we took a display case with plants and a live bumblebee colony, a video explaining research into honeybee behaviour, pollination research, and ecosystem services provided by pollinators and children's activities including colour a bumblebee, spot the difference between bees and hoverflies and a microscope with some examples of insects that provide ecosystem services. Members of the research group including Peter Kennedy, Rosalind Shaw and Juliet Osborne prepared the materials and attended the show. The show was present for 3 days during which large numbers of children and adults passed through the tent. Children and adults particularly enjoyed the live bumblebee colony where the bees could be seen both in the colony and then flying out and visiting plants in the display cage, many people commenting that they hadn't seen a bumblebee colony before.
Year(s) Of Engagement Activity 2017
 
Description Science Correspondent for professional practioners' newsletter 
Form Of Engagement Activity A magazine, newsletter or online publication
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Professional Practitioners
Results and Impact Recurring activity: Science Correspondent for beekeepers association newsletter writing regular pieces on recent research insights and current scientific literature.
Year(s) Of Engagement Activity 2015,2016,2017
 
Description Talk: BOAD Cornwall Beekeepers Event 2015 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Professional Practitioners
Results and Impact Talk to their Annual Event which has about 100 audience members of beekepers and interested general public- many questions and met with much enthusiasm. Beekeepers engaged in debate about future research funding proposal which they would like to co-create with us
Year(s) Of Engagement Activity 2015
 
Description Talk: Cheshire Beekeepers Annual Convention Oct 2015 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Professional Practitioners
Results and Impact Talk and Discussion - sparked interest to follow our research outcomes
Year(s) Of Engagement Activity 2015
 
Description Talk: Devon Apicultural Research Group 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Professional Practitioners
Results and Impact Talk and full discussion of research priorities and outcomes. Participants interested in being involved in co-creating future projects
Year(s) Of Engagement Activity 2015
 
Description Talk: Holsworthy Beekeepers Spring Convention 2016 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Professional Practitioners
Results and Impact Talk at Spring Convention of Holsworthy Beekeepers. Lively discussion afterwards
Year(s) Of Engagement Activity 2016
 
Description Tregothnan Cornwall Bee Summit - expert panel member 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Professional Practitioners
Results and Impact Lively debate and discussion after summit.

Sarah Newton, MP, hosted debate in House of Commons (Oct 2014) the week afterwards citing the summit conclusions as evidence of Need for national Pollinator Strategy
Year(s) Of Engagement Activity 2014
URL https://tregothnan.co.uk/about/news/