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.
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.
Publications
Arce A
(2016)
Impact of controlled neonicotinoid exposure on bumblebees in a realistic field setting
in Journal of Applied Ecology
Arce AN
(2018)
Foraging bumblebees acquire a preference for neonicotinoid-treated food with prolonged exposure.
in Proceedings. Biological sciences
Brahma A
(2022)
Larger, more connected societies of ants have a higher prevalence of viruses.
in Molecular ecology
Colgan T
(2021)
Genomic signatures of recent adaptation in a wild bumblebee
Colgan TJ
(2019)
Caste- and pesticide-specific effects of neonicotinoid pesticide exposure on gene expression in bumblebees.
in Molecular ecology
Colgan TJ
(2022)
Genomic Signatures of Recent Adaptation in a Wild Bumblebee.
in Molecular biology and evolution
Dragan MA
(2016)
GeneValidator: identify problems with protein-coding gene predictions.
in Bioinformatics (Oxford, England)
Favreau E
(2018)
Genes and genomic processes underpinning the social lives of ants
in Current Opinion in Insect Science
Jackson R
(2021)
Convergent evolution of a nutritional symbiosis in ants
López-Osorio F
(2020)
Healthy Pollinators: Evaluating Pesticides with Molecular Medicine Approaches.
in Trends in ecology & evolution
Manfredini F
(2022)
Social isolation and group size are associated with divergent gene expression in the brain of ant queens.
in Genes, brain, and behavior
Martinez-Ruiz C
(2020)
Genomic architecture and evolutionary antagonism drive allelic expression bias in the social supergene of red fire ants.
in eLife
Martinez-Ruiz C
(2020)
RNA/DNA extraction protocol v1
Moghul I
(2019)
Choosing the Best Gene Predictions with GeneValidator.
in Methods in molecular biology (Clifton, N.J.)
Nygaard S
(2015)
Ant genomics (Hymenoptera: Formicidae): challenges to overcome and opportunities to seize
in Myrmecological News
Nygaard Sanne
(2015)
Ant genomics (Hymenoptera: Formicidae): challenges to overcome and opportunities to seize
in MYRMECOLOGICAL NEWS
Pracana R
(2022)
Individual-based Modeling of Genome Evolution in Haplodiploid Organisms.
in Genome biology and evolution
Pracana R
(2017)
The fire ant social chromosome supergene variant Sb shows low diversity but high divergence from SB.
in Molecular ecology
Pracana R
(2017)
Fire ant social chromosomes: Differences in number, sequence and expression of odorant binding proteins
in Evolution Letters
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). We are submitting a manuscript documenting the genetic health of the common bombus terrestris bumblebee & identify using a novel approach what types of ecological and evolutionary pressures it has recently been subjected to. We have outlined a general approach for using molecular tools for polliantor health (publication in press in Trends in ECology and Evolution) |
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. Our use of high-resolution approaches for pollinator health is beginning to be noticed. We anticipate that their impacts will increase going forwards. They have already oriented funding at DEFRA/enviornment agency to further develop these approaches for aquatic organisms. |
Sector | Agriculture, Food and Drink,Chemicals,Digital/Communication/Information Technologies (including Software),Education,Healthcare,Government, Democracy and Justice |
Impact Types | Cultural Societal |
Description | Pollinator.health website |
Geographic Reach | National |
Policy Influence Type | Influenced training of practitioners or researchers |
URL | https://pollinator.health |
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 | 09/2019 |
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 | 05/2017 |
End | 04/2020 |
Description | Research England Policy Impact Funding |
Amount | £43,858 (GBP) |
Organisation | United Kingdom Research and Innovation |
Department | Research England |
Sector | Public |
Country | United Kingdom |
Start | 01/2022 |
End | 07/2022 |
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 | United Kingdom |
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 |
Description | Seirian Sumner collab |
Organisation | University College London |
Country | United Kingdom |
Sector | Academic/University |
PI Contribution | Joint PhD student with Prof Seirian Sumner |
Collaborator Contribution | PhD project cosupervision |
Impact | ongoing phd project of Alicja Witwicka. 2022 Mol Ecol paper. Others in prep |
Start Year | 2020 |
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 |
Company Name | Pragmatic Genomics |
Description | Pragmatic Genomics develops a range of data science software and provides data analysis, specialising in genomics data. |
Year Established | 2021 |
Impact | Customers in private (biotech, agroindustry), public and third sectors. |
Website | https://pragmaticgenomics.com/ |
Description | Outreach talk |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | Local |
Primary Audience | Public/other audiences |
Results and Impact | Gave a talk on how our work cna help pollinator declines at art gallery where artitst focused on our polliantors |
Year(s) Of Engagement Activity | 2019 |
URL | https://www.alkeschmidt.com/single-post/2019/08/31/SWARM-exhibition-and-events-update |