Behavioural and molecular responses to pesticide exposure in bumblebees
Lead Research Organisation:
Imperial College London
Department Name: Life Sciences
Abstract
With globally growing human populations there is ever increasing demand for higher agricultural yields. Pesticides are applied to maintain high crop yields, but we know little about the effects that current pesticide use has on non-target organisms including the beneficial pollinators that visit these crops. The most important of such pollinators are the social bees (e.g. honey bees and bumble bees) - but their populations have recently been declining, posing important risks for food security and the global economy. Pesticides have been implicated in these declines, yet to date there is a great paucity of data to show whether pesticide exposure at field levels is actually having an effect on bees.
Field level pesticide exposure is typically non-lethal to bees; so why should we be concerned? Recent studies have highlighted that pesticides approximating field levels may induce sublethal effects on individual bee behaviour. The concern is therefore that such effects at the individual level may have knock on effects to colony reproduction and survival, and this would explain observed bee declines. However, there are almost no studies that have set out to show whether this is indeed the case. Furthermore, we still lack an understanding about the manner in which foraging bees are affected at both the behavioural and molecular (genetic) level. The importance of understanding the subtle or large effects of pesticide exposure on foraging performance should not be underestimated: i) colony growth relies directly on efficient foraging and ii) any impairment to foraging performance has direct consequences on the successful pollination of crops and wild flowers. It is thus a research priority to know how a pesticide exposure landscape affects bee foraging behaviour, how this affects colony success, and ultimately how this shapes bee populations.
We propose to carry out five axes of research that will address these gaps in our knowledge. Our study system will be bumblebees (Bombus spp), as bumblebees are one of the most substantial wild insect pollinators in the landscape, as well as being used for greenhouse pollination. First we will determine whether pesticides reduce the abilities of bumblebees to carry out complex pollination tasks. Second, we will determine whether this in turn affects colony growth and reproductive success. Third, we will determine whether exposure to pesticides affects the yield of the crops bumblebees are pollinating. Fourth, using tools previously only available to cancer researchers, we will identify the molecular changes that occur in bees when they are exposed to pesticides. Finally, by performing genetic screening on five species of wild bumblebees sampled from across the UK we will determine the extent to which pesticides affect wild bumblebee populations. If impairment to foraging behaviour induced by pesticide exposure has an effect on colony fitness then we expect there to be a strong selective pressure shaping bee populations.
Field level pesticide exposure is typically non-lethal to bees; so why should we be concerned? Recent studies have highlighted that pesticides approximating field levels may induce sublethal effects on individual bee behaviour. The concern is therefore that such effects at the individual level may have knock on effects to colony reproduction and survival, and this would explain observed bee declines. However, there are almost no studies that have set out to show whether this is indeed the case. Furthermore, we still lack an understanding about the manner in which foraging bees are affected at both the behavioural and molecular (genetic) level. The importance of understanding the subtle or large effects of pesticide exposure on foraging performance should not be underestimated: i) colony growth relies directly on efficient foraging and ii) any impairment to foraging performance has direct consequences on the successful pollination of crops and wild flowers. It is thus a research priority to know how a pesticide exposure landscape affects bee foraging behaviour, how this affects colony success, and ultimately how this shapes bee populations.
We propose to carry out five axes of research that will address these gaps in our knowledge. Our study system will be bumblebees (Bombus spp), as bumblebees are one of the most substantial wild insect pollinators in the landscape, as well as being used for greenhouse pollination. First we will determine whether pesticides reduce the abilities of bumblebees to carry out complex pollination tasks. Second, we will determine whether this in turn affects colony growth and reproductive success. Third, we will determine whether exposure to pesticides affects the yield of the crops bumblebees are pollinating. Fourth, using tools previously only available to cancer researchers, we will identify the molecular changes that occur in bees when they are exposed to pesticides. Finally, by performing genetic screening on five species of wild bumblebees sampled from across the UK we will determine the extent to which pesticides affect wild bumblebee populations. If impairment to foraging behaviour induced by pesticide exposure has an effect on colony fitness then we expect there to be a strong selective pressure shaping bee populations.
Planned Impact
The pollination service that bee pollination provides has an economic value of >£300 million in the UK alone (>$150bn p.a. globally) Therefore, any study that can identify the factors causing bee declines and help mitigate it is fundamentally important for food security, our economy and the environment. There are thus numerous interested parties that would be interested:
1) It will provide important data to inform pesticide regulatory authorities on the ecotoxicological testing guidelines for application of specific pesticides in order to reduce the risk posed to beneficial pollinators. It will also provide data to better inform regulators about the appropriate duration that toxicity testing should be carried out for to detect chronic effects (if any). Currently, the guidelines for ecotoxicological testing of pesticides does not consider methods which would detect sublethal effects, and nor does it ask for testing to be longer than 96 hours.
2) The data will inform the EU about whether the current restriction of three of the seven neonicotinoids should lead to: i) a permanent ban; ii) a prolonged suspension; iii) a lifted suspension and return to previous application procedures; or iv) a lifted suspension but with modified application guidelines. Moreover, our tests will look at the other four un-restricted neonicotinoids which will tell us whether they appear to be better alternatives or pose a greater threat than those that are currently restricted.
3) We expect that work such as this has the potential to change policy, especially if we consider that our previous work (Gill et al. 2012, Nature) was used to debate and influence the EU moratorium.
4) As has been evident over the past year, there is large appeal of bees to the general public. For instance the press interest surrounding the decline of bees and its impact on food security, and the protest outside parliament in April 2013 about bees and the effects of neonicotinoids, undeniably supports this.
5) We will actively seek to communicate and build knowledge exchange relationships with pesticide regulatory directorates (to inform policy & application guidelines), environmental agencies and conservation trusts (to inform about the risks posed to beneficial pollinators), farming unions (to make aware which practices pose a threat to the pollination service their crops rely on), stakeholders and beekeepers (to help protect bees), and the general public (public awareness) to disseminate the results of our research in the most effective way.
6) The outreach offices (Imperial & QMUL) have also expressed interest in creating pamphlets to summarise our research to an audience which would comprise primarily of farmers and the general public.
1) It will provide important data to inform pesticide regulatory authorities on the ecotoxicological testing guidelines for application of specific pesticides in order to reduce the risk posed to beneficial pollinators. It will also provide data to better inform regulators about the appropriate duration that toxicity testing should be carried out for to detect chronic effects (if any). Currently, the guidelines for ecotoxicological testing of pesticides does not consider methods which would detect sublethal effects, and nor does it ask for testing to be longer than 96 hours.
2) The data will inform the EU about whether the current restriction of three of the seven neonicotinoids should lead to: i) a permanent ban; ii) a prolonged suspension; iii) a lifted suspension and return to previous application procedures; or iv) a lifted suspension but with modified application guidelines. Moreover, our tests will look at the other four un-restricted neonicotinoids which will tell us whether they appear to be better alternatives or pose a greater threat than those that are currently restricted.
3) We expect that work such as this has the potential to change policy, especially if we consider that our previous work (Gill et al. 2012, Nature) was used to debate and influence the EU moratorium.
4) As has been evident over the past year, there is large appeal of bees to the general public. For instance the press interest surrounding the decline of bees and its impact on food security, and the protest outside parliament in April 2013 about bees and the effects of neonicotinoids, undeniably supports this.
5) We will actively seek to communicate and build knowledge exchange relationships with pesticide regulatory directorates (to inform policy & application guidelines), environmental agencies and conservation trusts (to inform about the risks posed to beneficial pollinators), farming unions (to make aware which practices pose a threat to the pollination service their crops rely on), stakeholders and beekeepers (to help protect bees), and the general public (public awareness) to disseminate the results of our research in the most effective way.
6) The outreach offices (Imperial & QMUL) have also expressed interest in creating pamphlets to summarise our research to an audience which would comprise primarily of farmers and the general public.
People |
ORCID iD |
Richard Gill (Principal Investigator) | |
Nigel Raine (Co-Investigator) |
Publications
Smith DB
(2020)
Insecticide exposure during brood or early-adult development reduces brain growth and impairs adult learning in bumblebees.
in Proceedings. Biological sciences
Kenna D
(2019)
Pesticide exposure affects flight dynamics and reduces flight endurance in bumblebees.
in Ecology and evolution
Watrobska C
(2021)
Pollen Source Richness May Be a Poor Predictor of Bumblebee (Bombus terrestris) Colony Growth
in Frontiers in Insect Science
Watrobska C
(2020)
Pollen source richness may be a poor predictor of bumblebee colony growth
Description | Whilst the award period has finished, there are still a number of analyses being undertaken with key findings still to come (particularly on the molecular aspect of the project). Achieved so far: 1. Publication in J. Applied Ecology showing the effect that neonic pesticide exposure can have on bee colony reproduction, which was shown using a novel method of semi-field setup. 2. Publication in Proc. Roy. Soc. B showing that the risk of neonic exposure to bees is higher than previously thought, as foraging experiments showed bees exhibiting signs of addiction with chronic exposure. 3. Publication in Proc. Roy. Soc. B showing that pesticide exposure during larval development affects brain growth and predisposes adult workers to be poor learners 4. Publication in Molecular Ecology showing changes in gene expression when exposed to two specific neonic pesticides and that responses are different between castes. Ongoing (manuscripts in preparation) 1. Gut microbiome of multiple bee species across UK 2. Gut microbiome responses to pesticide exposure 3. Population genomics of a common bumblebee reveals signatures of selection from agricultural land-use change (under review) The genomic data and analytical pipelines are currently also informing another NERC funded project. |
Exploitation Route | Our findings are very important for risk assesment of pesticide use, and our work helped to inform the EFSA to implement the recent EU ban on three neonics . Management of honeybee hives, bumblebee colonies and conservation of wild bees can act on our findings Our methods can also be adopted by pesticide regulatory testing procedures, and it is of use for farmers, conservationists, apidologists (bee keepers) and land managers. The work still in preparation will provide us with an understanding of how agricultutral practices have shaped our bee population over the past century. |
Sectors | Agriculture, Food and Drink,Chemicals,Education,Environment,Manufacturing, including Industrial Biotechology,Other |
Description | Publication in Journal of Applied Ecology was considered in the EFSA review of the risk of neonicotinoids to bees leading to a EU moratorium. Andres Arce who was postdoc on this grant is currently a member of the academic panel advising on the new risk assessment guidance for the risk to insect pollinators posed by pesticide use. The current publications from this grant are being used to inform this process. Findings in the publication in Proc Roy Soc B show that neonicotinoid treated field may actually be attractive to bees, and is being considered by environmental policy when determine re-assessment of risk to bees, particularly post-Brexit. Publication in Mol Biol & Evol provides whole genome sequencing of wild bumblebees and revealed areas of the genome under selection. This provides a new molecular resource that is useful for other academics and genome biologists. |
First Year Of Impact | 2016 |
Sector | Agriculture, Food and Drink,Chemicals,Environment,Government, Democracy and Justice,Other |
Impact Types | Policy & public services |
Description | Helped inform the European Commission SEP 2020 future brief on the importance of pollinators for human wellbeing |
Geographic Reach | Europe |
Policy Influence Type | Citation in other policy documents |
Impact | My work helped inform policy on where focus shod be placed to support pollinator populations to support human wellbeing. Importance for nature and human well-being, drivers of decline, and the need for monitoring |
URL | https://op.europa.eu/en/publication-detail/-/publication/ddcb6a5e-ca33-11ea-adf7-01aa75ed71a1 |
Description | BES Large Research Grant |
Amount | £17,000 (GBP) |
Organisation | British Ecological Society |
Sector | Charity/Non Profit |
Country | United Kingdom |
Start | 03/2017 |
End | 09/2017 |
Description | Effects of urbanisation on bees |
Organisation | Royal Holloway, University of London |
Country | United Kingdom |
Sector | Academic/University |
PI Contribution | Co-supervised two BBSRC funded PhD students, and providing help through an advisory capacity |
Collaborator Contribution | Undertook empirical experiments looking at bee responses to land use and pesticide exposure, and modeling of foraging movements in bees. |
Impact | 1. Palmer et al. in prep. 2. DOI: 10.1007/s13592-020-00758-1 3. DOI: 10.1098/rspb.2018.0807 4. DOI: 10.1038/srep38957 |
Start Year | 2016 |
Description | Molecular responses to pesticide exposure in bees |
Organisation | Queen Mary University of London |
Department | School of Biological and Chemical Science QMUL |
Country | United Kingdom |
Sector | Academic/University |
PI Contribution | We are looking at population genomics and gene expression studies for multiple native bumblebee populations across the UK. My group carried out the field sampling, identifications, prepration, DNA extractions, and help with library preps for the molecular work to be undertaken, as well as controlled exposure assays. This has then fed into the work carried out by the collaborators. |
Collaborator Contribution | Managed the DNA and RNA sequencing and undertaken the bioinformatics required to address the questions posed. |
Impact | 1. Colgan et al. under review Genome Biology 2. DOI: 10.1111/mec.15047 3. DOI: 10.1098/rspb.2018.0655 4. DOI: 10.1111/1365-2664.12792 The collaboration is multi-disciplinary. |
Start Year | 2014 |
Description | Beekeepers Association meeting 2021 |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | Regional |
Primary Audience | Public/other audiences |
Results and Impact | Presented research on the risk of pesticide to bees |
Year(s) Of Engagement Activity | 2021 |
Description | Central Bekeepers association |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | Regional |
Primary Audience | Public/other audiences |
Results and Impact | Central Beekeepers association invited me as speaker to discuss the threats facing bees |
Year(s) Of Engagement Activity | 2016 |
Description | Imperial Science Breaks |
Form Of Engagement Activity | Participation in an activity, workshop or similar |
Part Of Official Scheme? | No |
Geographic Reach | National |
Primary Audience | Public/other audiences |
Results and Impact | Imperial Science Breaks to showcase our work studying the unsung heroes of agriculture. https://www.youtube.com/watch?v=MOrK0u_jIPA |
Year(s) Of Engagement Activity | 2020 |
URL | https://www.imperial.ac.uk/events/125601/science-breaks-unseen-organisms-and-unsung-heroes/ |
Description | Invited talk on bee research - CNRS |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Other audiences |
Results and Impact | Presented work to researchers at the CNRS in Toulouse, France |
Year(s) Of Engagement Activity | 2020 |
Description | Milan Expo |
Form Of Engagement Activity | A formal working group, expert panel or dialogue |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Public/other audiences |
Results and Impact | Milan Expo - Invited to the UK exposition (the Hive) and presented and discussed threats to insect pollinators |
Year(s) Of Engagement Activity | 2015 |
Description | POST meeting on understanding insect declines |
Form Of Engagement Activity | A formal working group, expert panel or dialogue |
Part Of Official Scheme? | No |
Geographic Reach | National |
Primary Audience | Policymakers/politicians |
Results and Impact | Parliamentary Office for Science & Technology. I contributed to a POST note and report on understanding insect declines, and then attended parliament to provide an expert opinion in using next-generation molecular techniques to study and monitor insects. |
Year(s) Of Engagement Activity | 2020 |
URL | https://post.parliament.uk/research-briefings/post-pb-0036/ |
Description | Royal Entomological Society Invited Speaker on Insect Declines |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Other audiences |
Results and Impact | nvited Speaker on Insect Declines - talked about my current work adressing this issue |
Year(s) Of Engagement Activity | 2019 |
Description | Royal Entomological Society special interest group |
Form Of Engagement Activity | Participation in an activity, workshop or similar |
Part Of Official Scheme? | No |
Geographic Reach | National |
Primary Audience | Other audiences |
Results and Impact | Using new technologies to study insects |
Year(s) Of Engagement Activity | 2015 |