Bee sensitivity to a century of agricultural land-use change

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

Abstract

The world's natural resources have been placed under significant pressure over the past century, due to the exponential growth rate of the global human population. This has resulted in a significant increase in agricultural land-use and subsequent loss of 'natural habitats', a pattern associated with high losses in biodiversity. Declines of insect pollinators, such as bumblebees, are of particular concern as their role in maintaining floral health and diversity is vital, and as agricultural crop pollinators they possess large economic benefits. Understanding threats to these populations is therefore of high priority.

Here we take the approach that to understand future threats and solutions we must understand the past, and that to accurately predict future patterns and risks to species, we must gain a better understanding of what is causing those changes. Unfortunately, archival data on insect pollinator abundance rarely goes back more than a couple of decades, and most have been collected in a haphazard way. To fill this knowledge gap we will take a novel approach in which, using a combination of DNA sequencing, morphological and phenological (life-history data looking at seasonal activity) measures, along with experimental test of pesticide resistance, we will test whether populations experiencing different agricultural land use change intensity show signatures of population declines and adaptation to these new agricultural environments (i.e. support for a causal relationship).

Here, we will study a large collection of historical bumblebee specimens from six leading natural history museums across the UK. The morphological and genomic data represented in these specimens holds the key to determining how variation in population size, body shape and genetic diversity have changed over the last century.

Recent advances in the recovery and analysis of ancient DNA, and developments in the resolution of CT scanning, will enable us to gain unprecedented and novel insights. By working with historical samples from locations that have undergone different amounts of agricultural land use change (for example differences between the east and west of UK) we can specifically test whether temporal changes occur, rather than relying on end point data.

It is widely considered that bumblebees are threatened by two of the major factors associated with agricultural intensification: the loss of flowers leading to reduced nutritional resource, and increased exposure to pesticides. However, to our knowledge the interactive effects of these have not been experimentally tested. This project will also conduct a controlled laboratory experiment to understand how changes to nutritional availability and pesticide exposure impact on colony growth and the production of new queens and males.

Planned Impact

The proposed project will provide results of interest not only to academics, but to a wide range of beneficiaries including: (i) policy makers (ii) agriculturists (iii) commercial parties relating to the chemical/pesticide industries (iv) conservationists and wildlife trusts (v) museums and (vi) the general public.

Bee pollination provides a service that has an economic value of >£300 million in the UK alone (>$150bn p.a. globally) thus identifying the factors causing bee declines is of fundamental importance. In relation to (i) policy makers, the project will provide data that can aid pesticide regulatory authorities by informing on how bees are coping in a pesticide exposure landscape. The data produced could also contribute to evidence considered by the EFSA on the risks of pesticide exposure to beneficial arthropods (primarily bees). The neonicotinoid pesticide under investigation in our proposed demographic pinch point experiment is currently under restrictions for use on flowering crops, therefore our findings may help to inform decisions on future applications. We believe that research in this field has the potential to change policy especially if we consider that previous work by Gill was used to debate and influence the EU moratorium, and has been presented at Parliament.

Land managers, farmers and beekeepers (ii) have a vested interest in the success of insect pollinators. Our proposed research could inform these parties regarding warning signs of future population crashes and future trends. It will also assist them to identify best agricultural practices and to develop mitigation strategies to benefit pollinators regarding pesticide application procedures. Moreover, by identifying specific detoxification genes this will be of broad use to (iii) ecotoxicologists and the chemical companies themselves (such as Syngenta).

Understanding the threats to insect pollinators, such as bees, is on the priority list of the International Platform of Biodiversity and Ecosystem Services (IPBES). Our findings can help to predict future trends of insect pollinators and other beneficial organisms that may inadvertently be affected by agricultural land use change and agricultural practices. It will also provide conservation groups (iv) with data on the regional population and community status of bees.

In relation to museums (v), our project would bring together curators and collections across the UK to address a grand challenge and reinforce a UK entomological collection network. The multiple museum collections involved will benefit from the genetic data, 3D reconstructions and morphological measurements that we will obtain, and intend to link (likely via QR codes), to each specimen. We envisage that these will be displayed for the visiting public (vi) in each of the respective museums. As has been evident over recent years, 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. We therefore hope that by understanding the past to predict the future this proposed research can assist with mitigating the threats to insect pollinators for conservation, future food security and general human welfare.

Publications

10 25 50
 
Description Currently have manuscript under invited re-submission:
Arce, Cantwell-Jones et al. Signatures of increasing environmental stress in bumblebee wings over the past century: Insights from museum specimens. J Animal Ecology.

Currently have manuscript under submission:
Mullin et al. Genome sequencing of museum insect specimens. Methods in Ecology & Evolution

Currently have manuscripts in preparation:
Arce et al. Phenological responses over the past century in bumblebees
Dixit et al. Bee and butterfly body size changes over the past century
Gill et al. Butterfly wing shape change reveals environmental pressures on insect pollinators

The project has been successful in collating digitized data on over 20K museum specimens.
Exploitation Route Currently collaborating with museum curators, records teams and findings will be of interest to conservation trusts, academics, land managers and policymakers.
Have been invited to speak at UK parliament about how to use molecular techniques and museum collections to understand insect pollinator losses.
Working on and a follow-up grant proposal to expand to other functional invertebrate groups.
Provided new digitized database for museum speicmens
Sectors Agriculture, Food and Drink,Chemicals,Education,Environment,Leisure Activities, including Sports, Recreation and Tourism,Government, Democracy and Justice,Culture, Heritage, Museums and Collections

 
Description Currently collaborating with natural history museums across the UK to provide added value to the public collection. Speaking at parliament about how to use molecular methods and museum collections to understand insect declines. Contributed to Insect Declines POSTnote 2020. Tullie House museum won an award, and used our project as a case study to support importance of public collection. NHM London wrote a piece on insect pollinator declines, and reported on our study using collections. Provided the platform for future grant proposals that are currently being written. Initiated collaboration with a US team (iDigBees).
First Year Of Impact 2018
Sector Agriculture, Food and Drink,Education,Environment,Leisure Activities, including Sports, Recreation and Tourism,Culture, Heritage, Museums and Collections,Other
Impact Types Cultural,Societal,Policy & public services

 
Description Contributed to a PostNote in insect declines
Geographic Reach National 
Policy Influence Type Implementation circular/rapid advice/letter to e.g. Ministry of Health
Impact This is under embargo until April 2020
 
Description CB Dennis Research grant
Amount £90,000 (GBP)
Organisation C.B. Dennis British Beekeepers' Research Trust 
Sector Charity/Non Profit
Country United Kingdom
Start 10/2023 
End 10/2026
 
Title First large-scale quantification study of DNA preservation in insects from natural history collections using genome-wide sequencing 
Description Insect declines are a global issue with significant ecological and economic ramifications. Yet we have a poor understanding of the genomic impact these losses can have. Genome-wide data from historical specimens has the potential to provide baselines of population genetic measures to study population change, with natural history collections representing large repositories of such specimens. However, an initial challenge in conducting historical DNA data analyses, is to understand how molecular preservation varies between specimens. Here, we highlight how Next Generation Sequencing methods developed for studying archaeological samples can be applied to determine DNA preservation from only a single leg taken from entomological museum specimens, some of which are more than a century old. An analysis of genome-wide data from a set of 113 red-tailed bumblebee (Bombus lapidarius) specimens, from five British museum collections, was used to quantify DNA preservation over time. Additionally, to improve our analysis and further enable future research we generated a novel assembly of the red-tailed bumblebee genome. Our approach shows that museum entomological specimens are comprised of short DNA fragments with mean lengths below 100 base pairs (BP), suggesting a rapid and large-scale post-mortem reduction in DNA fragment size. After this initial decline, however, we find a relatively consistent rate of DNA decay in our dataset, and estimate a mean reduction in fragment length of 1.9bp per decade. The proportion of quality filtered reads mapping our assembled reference genome was around 50 %, and decreased by 1.1 % per decade. We demonstrate that historical insects have significant potential to act as sources of DNA to create valuable genetic baselines. The relatively consistent rate of DNA degradation, both across collections and through time, mean that population level analyses - for example for conservation or evolutionary studies - are entirely feasible, as long as the degraded nature of DNA is accounted for. 
Type Of Material Database/Collection of data 
Year Produced 2022 
Provided To Others? Yes  
URL http://datadryad.org/stash/dataset/doi:10.5061/dryad.5mkkwh787
 
Title Thermal flight performance reveals impact of warming on bumblebee foraging potential 
Description The effects of environmental temperature on components of insect flight determine life-history traits, fitness, adaptability, and ultimately, organism ecosystem functional roles. Despite the crucial role of flying insects across landscapes, our understanding of how temperature affects insect flight performance remains limited. Many insect pollinators are considered under threat from climatic warming. Quantifying the relationship between temperature and behavioural performance traits allows us to understand where species are operating in respect to their thermal limits, helping predict responses to projected temperature increases and/or erratic weather events. Using a tethered flight mill, we quantify how flight performance of a widespread bumblebee, Bombus terrestris, varies over a temperature range (12-30oC). Given that body mass constrains insect mobility and behaviour, bumblebees represent a useful system to study temperature-mediated size-dependence of flight performance owing to the large intra-colony variation in worker body size they exhibit. Workers struggled to fly over a few hundred metres at the lowest tested temperature of 12oC, however flight endurance increased as temperatures rose, peaking around 25oC after which it declined. Our findings further revealed variation in flight capacity across the workforce, with larger workers flying further, longer, and faster than their smaller nestmates. Body mass was also positively related with the likelihood of flight, although importantly this relationship became stronger as temperatures cooled, such that at 12oC only the largest workers were successful fliers. Our study thus highlights that colony foraging success under variable thermal environments can be dependent on the body mass distribution of constituent workers, and more broadly suggests smaller-bodied insects may benefit disproportionately more from warming than larger-bodied ones in terms of flight performance. By incorporating both flight endurance and likelihood of flight, we calculated a simple metric termed 'temperature-mediated foraging potential' to gain a clearer understanding of how temperature may constrain colony foraging. Of our tested temperatures, 27oC supported the highest potential, indicating that for much of the range of this species, higher mean daily temperatures as forecasted under climate warming will push colonies closer to their thermal optimum for flight. Subsequently, warming may have positive implications for bumblebee foraging returns and pollination provision. 
Type Of Material Database/Collection of data 
Year Produced 2021 
Provided To Others? Yes  
URL http://datadryad.org/stash/dataset/doi:10.5061/dryad.18931zcxr
 
Title Toxic temperatures: Bee behaviours exhibit divergent pesticide toxicity relationships with warming 
Description Climate change and agricultural intensification are exposing insect pollinators to temperature extremes and increasing pesticide usage. Yet, we lack good quantification of how temperature modulates the sublethal effects of pesticides on behaviours vital for fitness and pollination performance. Consequently, we are uncertain if warming decreases or increases the severity of different pesticide impacts, and whether separate behaviours vary in the direction of response. Quantifying these interactive effects is vital in forecasting pesticide risk across climate regions and informing pesticide application strategies and pollinator conservation. This multi-stressor study investigated the responses of six functional behaviours of bumblebees when exposed to either a neonicotinoid (imidacloprid) or a sulfoximine (sulfoxaflor) across a standardised low, mid, and high temperature. We found the neonicotinoid had a significant effect on five of the six behaviours, with a greater effect at the lower temperature(s) when measuring responsiveness, the likelihood of movement, walking rate, and food consumption rate. In contrast, the neonicotinoid had a greater impact on flight distance at the higher temperature. Our findings show that different organismal functions can exhibit divergent thermal responses, with some pesticide-affected behaviours showing greater impact as temperatures dropped, and others as temperatures rose. We must therefore account for environmental context when determining pesticide risk. Moreover, we found evidence of synergistic effects, with just a 3°C increase causing a sudden drop in flight performance, despite seeing no effect of pesticide at the two lower temperatures. Our findings highlight the importance of multi-stressor studies to quantify threats to insects, which will help to improve dynamic evaluations of population tipping points and spatiotemporal risks to biodiversity across climate regions. 
Type Of Material Database/Collection of data 
Year Produced 2023 
Provided To Others? Yes  
URL http://datadryad.org/stash/dataset/doi:10.5061/dryad.9ghx3ffnf
 
Title Toxic temperatures: bee behaviours exhibit divergent pesticide toxicity relationships with warming 
Description Data, scripts and video produced from research 
Type Of Material Database/Collection of data 
Year Produced 2023 
Provided To Others? Yes  
Impact Lead to a publication in Global Change Biology 
 
Title UK museum specimen metadata and procrustes distance between left and right forewings, for five bumblebee species 
Description Data comprise the collection label details of museums specimens for five bumblebee species (Bombus hortorum, B. muscorum, B. lapidarius, B. pascuorum and B. sylvarum) from five UK museums (Natural History Museum (London), National Museums Scotland, Oxford University Museum of Natural History, Tullie House Museum and Art Gallery, and World Museum (Liverpool)). The details include species, collector, date collected, location, and caste. The location for each specimen was geotagged using Google Maps' Geocoding application programming interface. Each specimen had its left and right forewing landmarked, with the wing shapes aligned using a Procrustes alignment, and Procrustes distance between the wings calculated. The data came from a digitisation program as part of a NERC funded Standard Grant awarded to R. Gill (NE/P012574/1) and I. Barnes (NE/P012914/1). 
Type Of Material Database/Collection of data 
Year Produced 2022 
Provided To Others? Yes  
URL https://catalogue.ceh.ac.uk/id/2696535e-564a-4c6a-877e-515996fa97a1
 
Description Bee microbiome responses to pesticide exposure, and effects on the gut-brain axis 
Organisation Imperial College London
Department Faculty of Natural Sciences
Country United Kingdom 
Sector Academic/University 
PI Contribution Providing experimental setups and expertise
Collaborator Contribution Funding expense of colonies, and providing expertise on analysing bacterial community data.
Impact Kenna et al. in prep Arce et al. in prep
Start Year 2017
 
Description Bee sensitivity to a century of agricultural land-use change 
Organisation Natural History Museum
Country United Kingdom 
Sector Public 
PI Contribution Collating and cataloguing museum bee species. The NHM collaborators will extract DNA from these specimens
Collaborator Contribution Ancient DNA specialists
Impact None yet
Start Year 2017
 
Description Bee sensitivity to a century of agricultural land-use change 
Organisation University of Northampton
Country United Kingdom 
Sector Academic/University 
PI Contribution Collating and cataloguing museum bee species. The NHM collaborators will extract DNA from these specimens
Collaborator Contribution Ancient DNA specialists
Impact None yet
Start Year 2017
 
Description Building an entomological collection network 
Organisation Natural History Museum
Country United Kingdom 
Sector Public 
PI Contribution Oxford University Natural History Museum Cardiff Museum Natural History Museum London Tullie House Liverpool World Museum Scottish National Museum Great North Museum Manchester Natural History Musem
Collaborator Contribution Providing resources and allowing access to collections, and helping to develop a UK wide entomological database
Impact Arce et al. in prep Cantwell Jones et al. in prep. https://naturalhistorymuseum.blog/2018/08/13/digitising-british-bumblebees-digital-collections-programme/
Start Year 2017
 
Description Climate change impacts on bees 
Organisation Umea University
Country Sweden 
Sector Academic/University 
PI Contribution Fieldwork on bee interactions with Arctic plants
Collaborator Contribution Provided data on plant communities, collected climate data, and has provided logistical support and experimental resources to carry out the research.
Impact Cantwell-Jones et al. in prep. Podcast: https://www.podbean.com/ew/pb-cuxyz-b730ff Article: https://www.imperial.ac.uk/news/191967/audio-story-catching-arctic-bumblebees-study/
Start Year 2018
 
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 Genomes of museum bees 
Organisation Uppsala University
Country Sweden 
Sector Academic/University 
PI Contribution Coupling morphological data with genomic data of bumblebees
Collaborator Contribution Providing access to museum specimens, and producing molecular insigts into the evolution and ecology of bumblebees in Sweden.
Impact None as yet
Start Year 2019
 
Description Genomes of museum bees 
Organisation Vasa Museum, Stockholm
Country Sweden 
Sector Charity/Non Profit 
PI Contribution Coupling morphological data with genomic data of bumblebees
Collaborator Contribution Providing access to museum specimens, and producing molecular insigts into the evolution and ecology of bumblebees in Sweden.
Impact None as yet
Start Year 2019
 
Description Modelling bee colony dynamics and plant interactions 
Organisation Lund University
Country Sweden 
Sector Academic/University 
PI Contribution Undertaken some experiments, and provided empirical data
Collaborator Contribution Used the empirical data to inform mathematical models and understand bee ecology
Impact Ramos Rodrigues et al. in prep Cantwell-Jones et al. in prep Johansson & Gill under review
Start Year 2016
 
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 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 Interviews for National news 
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 Public/other audiences
Results and Impact Interviewed and filmed by two ITN groups, and this was broadcasted on ITV Evening News and Channel 4 Evening news, and thus received prime time audience.
Year(s) Of Engagement Activity 2022
 
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 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 PostNote - Talk at Parliament on Insect Declines 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Policymakers/politicians
Results and Impact How to use molecular methods to monitor insect populations
Year(s) Of Engagement Activity 2020
 
Description Presentation at IUSSI International Conference 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Other audiences
Results and Impact Presentation at IUSSI International Conference in San Diego on museum work
Year(s) Of Engagement Activity 2022
 
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 Society of Biology 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Other audiences
Results and Impact Threats to insect pollinators
Year(s) Of Engagement Activity 2019