Impact and mitigation of emergent diseases on major UK insect pollinators

Lead Research Organisation: University of Exeter
Department Name: Biosciences

Abstract

The mysterious death of thousands of honey bee colonies in the USA in the winter of 2005/06, termed Colony Collapse Disorder, focused media attention on the plight of bees, the world's primary pollinators. In the UK, both the honey bee and the 24 species of bumble bee play a major role in crop and wildflower pollination, and both have been suffering serious declines. Exotic (non-native) and newly emergent (native, but with increasing virulence) diseases are considered a major cause of decline in bees and consequently they are one of the greatest challenges to bees in the UK. The single-celled microsporidian 'fungus' Nosema ceranae is an exotic infectious disease of the honey bee that primarily attacks the gut of the bee. We have shown that it has spread worldwide, including the UK, within the last ca. 10 years, and it has been implicated in honey bee colony collapses in the USA (2005/06) and Spain (2007/08). Deformed Wing Virus (DWV) is the major disease organism associated with Varroa destructor mites of honey bees. This emergent disease replicates inside the bee, causing deformed wings and reduced longevity and is responsible for considerable honey bee colony mortality in the UK. Both disease organisms have recently been detected in bumble bees. Thus, both N. ceranae and DWV pose major threats to the UK's principal pollinators. Investigations of pollinator diseases typically focus on single-species interactions (one disease organism and one pollinator species). However, most parasites have multiple hosts and most hosts have multiple parasites. Here, we will take a multidisciplinary, ecological systems-based approach to understand the virulence (e.g. reduced longevity) and transmission of these two major disease organisms, N. ceranae and DWV, and detrimental synergies between them, on the UK's major pollination service providers: the honey bee and bumble bees. We will undertake laboratory epidemiological experiments (in which we look at the impact of a disease organism(s) on its host and the progression of disease from initial infection through to host mortality or recovery), state-of-the-art 'post-genomic' analyses and high-resolution radar tracking of individual insects to determine disease virulence and transmission. Using these data, we will parameterise a novel epidemiological model that will allow risk assessment of these emergent diseases on UK pollinators. Taking advantage of the complete genomes of both N. ceranae and DWV, we will undertake country-wide screening of pollinators to provide the evidence base of current disease strain prevalence. We will also refine innovative approaches for combating disease impacts. Specifically we will investigate the role of 'lactic acid bacteria' (the 'good guys' found naturally in healthy bee guts) and so-called RNAi technology (=RNA interference - short stretches of RNA that may interfere with viral replication inside a host) in curing bees of N. ceranae and DWV, which would provide long-term sustainable solutions to these disease organisms. For ca. £1.6 million (75% FEC), this interdisciplinary project will combine expertise from three leading UK bee and pollination research groups at Queen's University Belfast, Royal Holloway University of London and Rothamsted Research with mathematical modellers (Royal Holloway), pioneering microbiologists at the University of Lund (Sweden) and the world leader in RNAi technologies for bee diseases: Beeologics (USA). It will elucidate the impact and epidemiology of two increasingly important parasites on the UK's principal insect pollinators. Results will provide the evidence base for policy on disease mitigation strategies for government (conservation and agricultural advisory bodies) and major stakeholders (beekeepers, bumble bee importers). As well as serving as a model study of emergent pollinator diseases, project results will feed directly into husbandry practices and approaches to mitigate disease impact.

Technical Summary

Honey bees (Apis mellifera) and bumble bees (Bombus spp.) are the UK's principal pollinators yet both are in decline. Emergent infectious diseases are considered a major cause of bee decline. By combining theoretical modelling with empirical high-resolution evidence in an ecological systems approach, our £1.6 million (75% FEC) 3 year multidisciplinary project aims to understand the current and future threats posed by the UK's emergent and exotic honey bee pathogens on its major pollinators, and to develop innovative and sustainable mitigation strategies. We shall develop protocols for the culturing of DWV and N. ceranae so that single variants of these pathogens can be used in experimental investigation, allowing an explicitly experimental approach to host-parasite interactions. The UK's six common Bombus species will then be challenged with these pathogens to determine their susceptibility. Honey bees and bumble bees will then be challenged with one or both pathogens to determine synergies among multispecies parasite assemblages and host susceptibility, host immune response and host behaviour (pathogen transmission) measured in the lab and field as changes in host flight behaviour. These studies will be complemented by analysis of inter-specific host transmission of pathogens using state-of-the-art radar tracking of individual insects. A biologically realistic epidemiological model for a multi-parasite multi-eusocial-host system will be developed and used to refine experimental design and will be parameterised by results derived from these objectives. This model will provide risk assessment of DWV/N. ceranae and other emergent pathogens on the UK's major pollinator species. Two novel control methods, based on lactic acid bacteria of the bee gut and RNAi, will be tested for their efficacy. A countrywide survey of DWV and N. ceranae variants will provide the evidence base of current disease status and potential threats to the honey bee and to bumble bees.

Planned Impact

This interdisciplinary project will elucidate the impact and epidemiology of two increasingly important parasites, deformed wing virus (DWV) and the microsporidian Nosema ceranae, on the UK's major insect pollinators: honey bees and bumble bees. The impact of this project will be: 1) a substantially enhanced understanding of the interactions between pathogens and multiple pollinator hosts, knowledge that can be used to predict pollinator population changes and provide opportunities to mitigate parasite impacts with appropriate disease control strategies; and 2) a suite of new tools of vital importance in the study of pollinator pathology. In addition to the scientific community for whom high-impact research articles will be written, both areas will be of direct relevance to the following non-academic sectors: a) policy makers on sustainable pollination service provision, b) commercial and hobbyist beekeepers, c) NGOs and conservationists, d) farmers and industries involved in crop and food production and e) the wider public interested in the environment and pollinator conservation. a) Policy makers: We will use our contacts to ensure the implications of the project results are integrated into policies affecting bee and pollinator management. One route is via our close connections with EU policy makers (COLOSS and a briefing workshop for Members of the European Parliament on pollination and bees). b) Beekeepers: We will speak at beekeeping events, write for beekeeper newsletters and, specific to this project, we will invite regional beekeeping organisations to Rothamsted to see the radar in action (in 2011). We will also present our work at Apimondia, the international congress held specifically to disseminate research results to beekeepers. Through a public participation campaign, we shall engage beekeepers in assessing the risks posed by N. ceranae. c) NGOs and conservationists: We will engage with conservation organisations like Bumble Bee Conservation Trust and Bees Wasps and Ants Recording Society though data sharing and talks at their annual meeting. We will publicise results in targeted articles e.g. in British Wildlife, and dedicated leaflets. d) Farmers and associated industries: Rothamsted Research Association provides a forum for informing and engaging farmers and farming industries, and Osborne's team arrange regular farmer visit days to explain their research. One of these events incorporating this project will be held in 2012. e) General public: We have 15 years experience of disseminating results through the media (television, newspaper and radio) and we will extend these activities to incorporate this project and its results. Rothamsted holds Open Weekends showcasing their science to the public, and we will use this forum to inform on this project. Website: Of benefit to all stakeholders will be a project website. It will outline our research and provide opportunities for the public to engage with us. It will also publicise the prevalence and distribution of disease variants across bee species and will link to relevant NGOs and the new cross research council website on Food Security. All stakeholder event: In 2013, we shall stage an event either at Rothamsted or hosted by the Royal Entomological Society to bring together all stakeholders listed above for a workshop discussing the results of the project, inviting feedback and stimulating initiatives for disease management in wild and domesticated pollinators. Outside the project: We will engage with potential collaborators through data sharing, ensuring that our survey data on parasite distribution and abundance are available to organisations such as the National Bee Unit, FERA, and COLOSS. Exploitation: The project may generate significant exploitable results of considerable economic importance. If innovative control methods are successful, we will as a matter of priority engage with subcontractors and potential funders to undertake field-scale trials.
 
Description This grant was part of a collaborative project with Prof R Paxton (Belfast, Halle) and Prof M Brown (RHUL) and this statement reports on the whole project. Our overarching aim was to understand whether and how interactions among two emerging insect pathogens, deformed wing virus (DWV) and a spore-forming microorganism of the gut (a fungus-like microsporidian called Nosema ceranae or N. ceranae), impacted their known host, the honey bee. Further, we set out to determine the extent to which these pathogens also impacted other important insect pollinators of the UK, the bumble bees, and how they could be controlled in hosts. Our project partners successfully developed methods for rearing pathogens in the laboratory, and then we undertook a large body of experimental research, both in the laboratory under tightly controlled setting, and in the field using advanced radar technology, to determine how important each pathogen, alone and in combination, impacts these pollinator insects. We also developed novel mathematical models - informed by our empirical data - that can predict the impact of pathogens on social bees. We have 7 key findings:

1. Both DWV and N. ceranae are pathogen for honey bees. Contrary to our original hypothesis, they seem not to interact synergistically in elevating mortality of honey bees in the laboratory. Under most circumstances, DWV is far more virulent than N. ceranae for honey bees.

2. In a stressful field setting, the impact of both pathogens may be greater than that seen in the benign laboratory. Radar tracking demonstrates the difficulty faced by honey bees when orientating and flying if they are infected with either pathogen. [This was a key finding in our part of the project].

3. A novel method of control of pathogens, feeding with naturally occurring Lactic Acid Bacteria, provides health benefits for the honey bee, but they do not give specific benefits to hosts in combatting DWV and N. ceranae.

4. Theoretical modelling demonstrates that pathogens and other stressors such as pesticides may cause sudden collapse of social insect colonies when they suffer from on-going insult by these factors.

5. Both pathogens impact bumble bees, but again DWV has far greater impact on its host.

6. DWV is at an extremely high prevalence in British honey bees.

7. Pathogens of the honey bee may 'spill over' into bumble bees, and vice versa, with potentially devastating consequences for populations of both managed (honey bee) and largely unmanaged (bumble bee) pollinator populations.
Exploitation Route Policymakers may use our results in their formulation of evidence-based policy in relation to the importation, movement and stocking of managed pollinators. For bee-keepers, our results suggest that greater attention needs to be paid to management to reduce DWV pathogen loads, probably by reducing the number of Varroa mite pests in colonies. Conservationists, NGOs and the general public need to be aware of the risks that pathogens represent for pollinator numbers, and the potential that exists for inter-host transfer of pathogens. Our research should also motivate the scientific field to study the role of pathogens in regulating insect pollinator populations, and how virulence might evolve in a multi-host multi-pathogen system that is insect pollinators and their microbial associates.
Sectors Agriculture, Food and Drink,Environment

URL http://beediseases.org.uk/
 
Description The results of this project have gained widespread acknowledgement, such that further projects have been funded to look at the transfer of diseases between managed honeybees and bumblebees in the UK. Beekeepers are also talking about these results (social media; newsletters; conventions), in debate and considering best practice to keep their colonies healthy.
First Year Of Impact 2015
Sector Agriculture, Food and Drink,Environment
Impact Types Cultural

 
Description Expert advice at Bee Health Summit on the National Pollinator Strategy, Westminster
Geographic Reach National 
Policy Influence Type Participation in a guidance/advisory committee
Impact The National Pollinator Strategy has been published and is being implemented over the next 5 years to promote and conserve pollinator communities
 
Description Pollinator for Policy Workshop, London 2012
Geographic Reach National 
Policy Influence Type Participation in a guidance/advisory committee
Impact This workshop contributed to the development of the National Pollinator Strategy for the UK
 
Description C.B. Dennis British Beekeepers' Research Trust
Amount £15,000 (GBP)
Organisation C.B. Dennis British Beekeepers' Research Trust 
Sector Charity/Non Profit
Country United Kingdom
Start 09/2014 
End 03/2015
 
Description IPI consortium 
Organisation Martin Luther University of Halle-Wittenberg
Country Germany 
Sector Academic/University 
PI Contribution This project was a collaborative project between these organisations. Professor Robert Paxton was the lead P.I. University of Exeter & Rothamsted Research jointly addressed specific objectives 3 & 4 on transmission of bee disease and behaviour in the project
Collaborator Contribution This project was a collaborative project between these organisations. Professor Robert Paxton was the lead P.I.
Impact See outcomes of projects
Start Year 2011
 
Description IPI consortium 
Organisation Queen's University Belfast
Country United Kingdom 
Sector Academic/University 
PI Contribution This project was a collaborative project between these organisations. Professor Robert Paxton was the lead P.I. University of Exeter & Rothamsted Research jointly addressed specific objectives 3 & 4 on transmission of bee disease and behaviour in the project
Collaborator Contribution This project was a collaborative project between these organisations. Professor Robert Paxton was the lead P.I.
Impact See outcomes of projects
Start Year 2011
 
Description IPI consortium 
Organisation Rothamsted Research
Country United Kingdom 
Sector Academic/University 
PI Contribution This project was a collaborative project between these organisations. Professor Robert Paxton was the lead P.I. University of Exeter & Rothamsted Research jointly addressed specific objectives 3 & 4 on transmission of bee disease and behaviour in the project
Collaborator Contribution This project was a collaborative project between these organisations. Professor Robert Paxton was the lead P.I.
Impact See outcomes of projects
Start Year 2011
 
Description IPI consortium 
Organisation Royal Holloway, University of London
Country United Kingdom 
Sector Academic/University 
PI Contribution This project was a collaborative project between these organisations. Professor Robert Paxton was the lead P.I. University of Exeter & Rothamsted Research jointly addressed specific objectives 3 & 4 on transmission of bee disease and behaviour in the project
Collaborator Contribution This project was a collaborative project between these organisations. Professor Robert Paxton was the lead P.I.
Impact See outcomes of projects
Start Year 2011
 
Description BBC 4 Hive Alive 
Form Of Engagement Activity A press release, press conference or response to a media enquiry/interview
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Media (as a channel to the public)
Results and Impact TV program on bee biology incl. radar tracking of OF; invited to cover the radar work by Lars Chittka, who was approached by the BBC

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Year(s) Of Engagement Activity 2010,2014
 
Description BBC Horizon Special: What is killing our bees 
Form Of Engagement Activity A press release, press conference or response to a media enquiry/interview
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Media (as a channel to the public)
Results and Impact Program on bee decline featuring among others also Randolph Menzel, Dave Goulson, and Lin Field.

Radio interviews to promote the program
Year(s) Of Engagement Activity 2013
 
Description BBC Inside Out: TV piece with artist Kurt Jackson 
Form Of Engagement Activity A press release, press conference or response to a media enquiry/interview
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact Appearance on TV sparked questions about bumblebee ecology and diseases

*
Year(s) Of Engagement Activity 2015
 
Description British Beekeepers Association Annual Convention 2015: 2 Talks & poster on stand 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? Yes
Geographic Reach National
Primary Audience Public/other audiences
Results and Impact Talks sparked questions and discussion
Posters led to direct engagement with individuals throughout the convention

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Year(s) Of Engagement Activity 2015
 
Description EURBEE 2014: There and back again? - The effects of emergent pathogens on honeybee orientation flights 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Type Of Presentation paper presentation
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Presented talk as part of the 'effects of stressors on behaviour of bee pollinators' workshop, Murcia Spain

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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 Insect Pollinator Initiative Dissemination Event october 2014 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Professional Practitioners
Results and Impact Very important networking and communication event with key group of stakeholders

Further liaison with stakeholders about implementation of the National Pollinator Strategy
Year(s) Of Engagement Activity 2014
 
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 Phone interview for El Pais newspaper article "Effects of pathogens on honeybee flight behaviour" 
Form Of Engagement Activity A press release, press conference or response to a media enquiry/interview
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Media (as a channel to the public)
Results and Impact Phone interview for El Pais newspaper article "Effects of pathogens on honeybee flight behaviour"

*
Year(s) Of Engagement Activity 2014
 
Description Podcast on Planet Earth NERC website: Parasites stop bees finding their way home 
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 Media (as a channel to the public)
Results and Impact Stephan Wolf interviewed for Planet Earth podcast, publicising the PLoS one paper.

Triggered some further press enquiries about the work
Year(s) Of Engagement Activity 2014
URL http://planetearth.nerc.ac.uk/multimedia/story.aspx?id=1766
 
Description Talk: Bromley Beekeepers "Effects of pathogens on honeybee flight behaviour" 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Public/other audiences
Results and Impact Talk to Bromley beekeepers "Effects of pathogens on honeybee flight behaviour"

*
Year(s) Of Engagement Activity 2014
 
Description Talk: Hertfordshire Beekeepers "Effects of pathogens on honeybee flight behaviour" 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact Invited to speak at the Hertfordshire beekeepers "Effects of pathogens on honeybee flight behaviour"

Positive audience response
Year(s) Of Engagement Activity 2013
 
Description Talk: Learning from Nature: Bees and Pollination 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Schools
Results and Impact Talk and Workshop to Year 6 students at Dartmouth Academy

Very enthusiastic participatory school children gained knowledge.
Year(s) Of Engagement Activity 2013
 
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/