Behavioural and molecular responses to pesticide exposure in bumblebees.

Lead Research Organisation: Queen Mary, University of London
Department Name: Sch of Biological and Chemical 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.

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.

Publications

10 25 50
 
Description We found that:
1. Pesticides differently affect queens and workers in bumblebees. Furthermore, different pesticides (within the same group of neonicotinoids that target the same receptor) have different effects on gene activity. (Colgan et al Mol Ecol in press)
2. We co-demonstrated that, once exposed, bumblebees go out of their way to get more pesticide - similar to developing an addiction (Proceeding B 2018).
Exploitation Route Many researchers working on genomics of wild organisms face similar challenges for analysing data. The tools we have created to do this are already greatly helping others with similar datasets.

We anticipate others to make strong use of the genomic sequences and the biological insight our project will provide.

We are following up with multiple additional analysis
Sectors Agriculture, Food and Drink,Chemicals,Education,Environment,Pharmaceuticals and Medical Biotechnology,Other

 
Description Non-academic impacts: During field work, we interacted with many members of the public - to whom we explained the rationale and funding mechanism for our research on pollinators, as well as their importance for the ecosystem. Additionally, our software outputs have had visibility across non-NERC sciences including in the software development world. Our published work received extensive visibility (see altmetric) and citations - which will have fed into recent debates on the use of pesticides. One of the policy impacts of this, is that several commonly used neonicotinoid pesticides were banned for outdoor use by the EC in 2018, with other pesticides still under review.
First Year Of Impact 2015
Sector Agriculture, Food and Drink,Chemicals,Digital/Communication/Information Technologies (including Software),Education,Healthcare,Government, Democracy and Justice
Impact Types Cultural,Societal

 
Description BBSRC NPIF Case Studentship
Amount £107,034 (GBP)
Funding ID BB/S507556/1 
Organisation Biotechnology and Biological Sciences Research Council (BBSRC) 
Sector Public
Country United Kingdom
Start 12/2018 
End 11/2022
 
Description Marie Sklodowska Curie Incoming Fellowship H2020-MSCA-IF-2018
Amount € 224,933 (EUR)
Organisation European Commission H2020 
Sector Public
Country Belgium
Start 10/2019 
End 10/2021
 
Description Marie Sklodowska Curie Incoming Fellowship H2020-MSCA-IF-2018 (another)
Amount € 212,933 (EUR)
Funding ID EvolvAnt 
Organisation European Commission H2020 
Sector Public
Country Belgium
Start 03/2020 
End 02/2022
 
Description Marie curie
Amount € 221,606 (EUR)
Funding ID 623713 
Organisation European Commission 
Department Seventh Framework Programme (FP7)
Sector Public
Country European Union (EU)
Start 02/2015 
End 02/2017
 
Description NE/P012574/1
Amount £648,559 (GBP)
Funding ID NE/P012574/1 
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 06/2017 
End 04/2020
 
Title Flo 
Description Software: flo to transfer gene predictions from one genome assembly to another genome assembly (from same species) 
Type Of Material Technology assay or reagent 
Year Produced 2016 
Provided To Others? Yes  
Impact Makes it easier to use new (higher quality) genome assemblies 
URL https://github.com/wurmlab/flo
 
Description Collab Marc Robinson Rechavi 
Organisation Swiss Institute of Bioinformatics (SIB)
Country Switzerland 
Sector Charity/Non Profit 
PI Contribution New collaboration - we obtained samples, dissected, extracted RNA. We are leading bioinformatic analysis
Collaborator Contribution Partner contribtued funds for field sampling (which we did), and for gene expression sequencing. They are helping with bioinformatic analysis
Impact not yet
Start Year 2016
 
Description Fellowship at Alan Turing Institue for data science and artificial intelligence 
Organisation Alan Turing Institute
Country Unknown 
Sector Academic/University 
PI Contribution I am a fellow - interacting with data-centric peers from other fields
Collaborator Contribution Expertise of others in data science techniques - carrying over expertise into our research. -> synergistic grant application and project ideas.
Impact Collaborative BBSRC grant submission
Start Year 2018
 
Title GeneValidator 
Description Genomes of emerging model organisms are now being sequenced at very low cost. However, obtaining accurate gene predictions remains challenging. Even the best gene prediction algorithms make substantial errors, leading to further erroneous analysis. Therefore, many predicted genes need to be visually inspected and manually curated, a time consuming process. Here we propose GeneValidator, a tool to identify problematic gene predictions and to guide curation efforts. For each newly predicted protein-coding gene, GeneValidator finds similar sequences in databases of known genes and performs general gene-characteristic comparisons. The resulting report highlights differences between each putative protein-coding gene and similar genes from the database. This allows rapid identification of curation need and guides curators in performing their work. We thus expect GeneValidator to greatly accelerate and enhance the work of biocurators and researchers working with recently sequenced genomes. 
Type Of Technology Software 
Year Produced 2014 
Open Source License? Yes  
Impact Publication is in prep. 
URL https://github.com/monicadragan/GeneValidator/
 
Title Sequenceserver 
Description Makes it easier to perform BLAST 
Type Of Technology Software 
Year Produced 2012 
Open Source License? Yes  
Impact (development has continued). 
URL http://www.sequenceserver.com