Behavioural and molecular responses to pesticide exposure in bumblebees

Lead Research Organisation: Imperial College London
Department Name: Life Sciences


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.

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.


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Description Whilst the award has not finished, there are still analyses and outputs being undertaken with key findings still to come (particularly on the molecular aspect of the project). Here is what we have 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. of Royal Society 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. Manuscript in preparation looking at bee feeding habits and foraging performance by individual colony members under the influence of pesticide
4. At least two manuscripts in preparation studying the microbiome of pesticide exposed bees in the lab, and microbiome profiles of field collected wild bees.
5. Publication in Molecular Ecology presenting the results of a transcriptome experiment showing that two neonic pesticides change the expression of up to 50 genes involved in important biological processes, with queens and workers responding differently.
6. Manuscript in preparation looking at transcriptomic genes expression profiles of controlled age workers exposed to single and combinatorial pesticide exposure
7. Two manuscripts in preparation investigating the population genomics of UK bumblebee species

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,Environment,Manufacturing, including Industrial Biotechology,Other

Description Publication in Journal of Applied Ecology is currently being considered in the EFSA review of the risk of neonicotinoids to bees.
First Year Of Impact 2016
Sector Agriculture, Food and Drink,Chemicals,Environment
Impact Types Policy & public services

Description BES Large Research Grant
Amount £17,000 (GBP)
Organisation British Ecological Society 
Sector Learned Society
Country United Kingdom
Start 03/2017 
End 09/2017
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 Arce et al. 2017 Journal of Applied Ecology; Arce et al. re-submisison Proc B; Colgan et al. in prep; Colgan*; Arce* et al. in prep; The collaboration is multi-disciplinary.
Start Year 2014