A systems approach to understanding the impacts of sublethal doses of neonicotinoids on bumblebee and honeybees

Lead Research Organisation: University of Sussex
Department Name: Sch of Life Sciences

Abstract

Neonicotinoid insecticides are now among the most widely used pesticides in the world, and are routinely used to protect a range of flowering crops such as oilseed rape and sunflowers against herbivores. In the UK, 1.27 million ha of crops were treated with neonicotinoids in 2010, with clothianidin, imidacloprid and thiamethoxam being the most frequently used types. Most are used as a seed-dressing, with the crop plant absorbing the compound as it grows, and hence becoming protected against herbivorous pests. Neonicotinoids are also used as foliar sprays on soft fruit crops, and are widely sold as sprays or granules for garden use on flowers, fruit and vegetable crops. As they are systemic chemicals, low concentrations of neonicotinoids are found in nectar and pollen of treated crops, and hence they are consumed by pollinators. They are also water soluble and persistent, so that detectable quantities are found in hedgerow / field margin wildflowers near treated crops.

Evidence is mounting that exposure of bees to neonicotinoids produces sublethal effects such as reduced navigational ability that would not be detected in laboratory assays, or in field trials where hives are placed immediately adjacent to a treated flowering crop. They are only apparent when bees are foraging at distance across the landscape, as occurs in nature. A recent study by the lead PI demonstrated that exposure of bumblebee nests to levels of imidacloprid which are known to occur in the nectar and pollen of seed-treated oilseed rape resulted in an 85% reduction in output of new queens (Whitehorn et al. 2012). A substantial proportion of both wild bumblebee nests and managed honeybee colonies are likely to be within foraging range of a treated, flowering crop, so it seems likely that this class of insecticide may be contributing substantially to the much-discussed declines in wild bee populations. There is an urgent need to understand the sublethal impacts of neonicotinoids on behaviour and colony-level performance of bumblebees under field conditions.

This project will quantify the levels of neonicotinoids found in crops and wildflowers in UK arable farmland, and feed these into landscape maps of the distribution of floral resources (produced in a parallel project, BB/J014753/1, starting 2013). We will quantify the doses of neonicotinoids that honeybee and bumblebee colonies are exposed to when naturally foraging in farmland, before going on to assess the likely impacts of this exposure on bumblebee colony performance. Exposure and impacts will be examined by both empirical studies and modelling approaches. Drs Osborne and Becher have developed an integrative model of a honeybee colony, which predicts forager behaviour and colony performance when placed into a real or simulated landscape. In project BB/J014753/1 we will develop a version of this model for bumblebee colonies. These models will enable us to predict where both honeybee and bumblebee workers will forage, and thus predict their exposure, which will be compared to that received by real nests placed in the landscape. We will then examine whether exposure to neonicotinoids at realistic field levels alters or impairs foraging behaviour using Rothamsted's unique harmonic radar facility. These data will be used to develop a sub-model for both honeybees and bumblebees which includes impacts of neonicotinoids in predictions of colony success, which will be tested with real colonies of bumblebees in field experiments, and can be used as a risk assessment tool by users. Finally, the data and model results will enable us to develop management recommendations to minimise the impacts of neonicotinoids on both managed honeybees and wild bumblebee populations.

Technical Summary

Neonicotinoid insecticides are used to protect a range of crops such as oilseed rape and cereals against herbivores. They are also used as foliar sprays on soft fruit crops and are widely sold for garden use on flowers, fruit and vegetable crops. Evidence is mounting that exposure of bees to neonicotinoids produces sublethal effects such as reduced navigational ability that are not detected in laboratory assays or in field trials where hives are adjacent to a treated flowering crop.

This project will quantify the levels of neonicotinoids found in crops and wildflowers in UK arable farmland, and feed these into landscape maps of the distribution of floral resources (produced in a parallel project, BB/J014753/1, starting 2013). We will quantify the doses of neonicotinoids that honeybee and bumblebee colonies are naturally exposed to, before going on to assess the impacts of this exposure on bumblebee colony performance. Exposure and impacts will be examined by both empirical studies and modelling approaches. An existing integrative model of a honeybee colony development, which predicts forager behaviour and colony performance, is being adapted for bumblebees in project BB/J014753/1. These models will enable us to predict where both honeybee and bumblebee workers will forage, and thus predict their exposure, which will be compared to that recieved by real nests placed in the landscape. We will then examine whether exposure to neonicotinoids at realistic field levels alters or impairs foraging behaviour using Rothamsted's unique harmonic radar facility. These data will be used to develop a sub-model for both honeybees and bumblebees which includes impacts of neonicotinoids in predictions of colony success, which will be tested with real colonies of bumblebees in field experiments. We will use the model simulatons to develop management recommendations to minimise the impacts of neonicotinoids on both managed honeybees and wild bumblebee populations.

Planned Impact

The impact of this project will be a substantially enhanced understanding of the role of sublethal exposure to neonicotinoids on the predominant pollinator groups, honeybees andbumblebees, in arable farmland; and a modelling tool to help in the risk assessment process. The project has clear relevance for understanding how pest management decisions impact on the provision of a vital ecosystem service (pollination). It aims to produce management recommendations which will mitigate negative effects and ultimately help to enable us to farm sustainably. It is therefore of high relevance to many stakeholders. Pollination is crucial for farmers, and our results will help ensure that bees can be deployed practically and sustainably to provide good yields for appropriate crops. This will become increasingly important as summers become warmer and drier and new crop species are planted e.g. sunflower, which depend on insect pollination but are generally treated with neonicotinoids.


Who will benefit and how?

Policy makers (e.g. Defra)
The project will provide large new datasets, and an interactive web-based tool modelling bee colony development, to aid policy makers and regulators in regional, national, EU and other agencies. These will serve as the basis for the development of sound policies with respect to pesticide use and pollination, as well as practical advice and recommendations to practitioners in the land-based industries.

Farmers, beekeepers and the agri-food industry
Our data will provide much-needed information on the safety of this class of agrochemical for both managed and wild bee populations, and will provide practical advice on how best to balance the clear conflict between pest control and pollination. This is particularly acute in soft-fruit farming where farmers currently buy bumblebee nests while using systemic insecticides. The lead PI has previously given talks to soft fruit growers at the James Hutton Institute at their annual event where growers are invited to meet and talk to researchers, and this approach will be used again. Similarly, the lead PI has spoken at the annual British Beekeepers Association conference, and writes a regular column for their newsletter, and both methods will be used to convey the results of this project to the beekeeping community. Three large agrochemical companies have actively been requesting the development of a model to predict exposure to neonicotinoids and subsequent effects at the colony level so this project provides an opportunity to contribute to this, independently, with the results being directly useful to the industries.

The NGO community: wildlife, conservation and environmental organisations and advisors.
Conservation organisations and stakeholders, such as Natural England, British Trust for Ornithology, the RSPB, The Game and Wildlife Conservation Trust, Butterfly Conservation, Bumblebee Conservation Trust and the British Beekeepers Association already collaborate with us and utilise the results we publish to enhance public awareness and advise land managers.

The public
The public at large are fascinated by bees and pollination, and rely on them for production of food to ensure a healthy and balanced diet. The applicants have excellent track records in reaching a wide audience with high profile and exciting science, via talks, specific events (workshops, Open Days, Hampton Court Flower show exhibits etc) and all forms of media (web, press, radio, television). We will continue to use all these types of communication to maximise impact. Enhancing public awareness and understanding of such issues is likely to play a key role in influencing policy makers to adopt appropriate changes.

Publications

10 25 50
 
Description We have quantified levels and routes of exposure of honeybees and wild bumblebees to pesticides commonly used in arable farming, with a particular focus on neonicotinoids. We simultaneously assessed exposure of bumblebee nests placed in urban areas, for comparison. The EU moratorium on use of neonicotinoids in flowering crops began during our study, providing us with a unique opportunity to evaluate the effect of the ban on exposure of bees. This work is now complete, and published at Nicholls et al. 2018, Env. Sci. Technol. 52, 9391-9402. In brief, we found that the ban did significantly reduce exposure of bees in farmland, although neonicotinoids and many other pesticides were still detected in food stores. Bees in urban areas were also exposed to neonicotinoids and other pesticides, and this exposure did not fall as a result of the ban.

We also examined effects of pesticides on bee health, some of which has since been published, suggesting that some solitary bees are not affected by field-realistic expsoure to neonicotinoids (Nicholls et al. 2017, PeerJ 5 e3417), where as the bumblebee B. terrestris is (Dance et al 2017 Ecotoxicoloy & Env. Safety 139: 194-201).

Our data on bee exposure and impacts of pesticides was fed into predictive, agent-based models developed at the University of Exeter which allow us to make more general, testable predictions about impacts of pesticides on colony growth and pollination service provision. The models were recently published as Becher et al. 2018 J Appl Ecol.
Exploitation Route The predictive model will allow us to quantify how altering pesticide will alter bumblebee populations in farmland, and how this will alter pollination, and thus should be of value to all interested in crop production, wild bee conservation, or conservation of wild flower communities.

Our data on pesticide exposure of bees in farmland is likely to have influenced the recent EU decision to ban three neonicotinoids.
Sectors Agriculture, Food and Drink,Environment

 
Description The findings from this project have helped to shape the conservation strategies of the Bumblebee Conservation Trust, an organisation that I set up in 2006 and was chair of the board of trustees of until 2011. The findings have also been explained to the public in more than 150 talks given to members of the public by the PI, at diverse locations and events including beekeeper meetings, local wildlife trusts, farmer associations, gardening associations and science and literary festivals. They have also informed a large number of popular science articles and information provided in media interviews. They are mentioned in my popular science books, A Sting in the Tale, and A Buzz in the Meadow, and have been described to policy makers in talks given in the Houses of Parliament, US Congress, Paris Senate and Ontario State Government. They form the basis of practical advice given out to policy makers, gardeners and farmers as to how to conserve wild bee populations, and as to the impacts of pesticides on bees.
First Year Of Impact 2014
Sector Agriculture, Food and Drink,Environment
Impact Types Societal,Economic,Policy & public services

 
Description pesticide policy
Geographic Reach Multiple continents/international 
Policy Influence Type Citation in other policy documents
Impact Our research was cited as one of two papers which triggered the European Food Standards Agency to launch an enquiry into the impacts of neonicotinoid pesticides on bees. This enquiry led to a vote on a 2 year moratorium on the use of these pesticides across the EU, which was passed by the European Parliament in 2013. As a result of this same research I was invited to visit USA and give a talk to the Fish & Wildlife Service on this issue. They have since banned neonicotinoids in all areas of the USA under their management.
 
Description Interviews on Radio, TV or Newspaper 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact I have given hundreds of media interviews over the last few years, resulting in appearances on radio (e.g. Radio 4 Farming Today and the Today Programme, National Radio in Canada, Australia and New Zealand), television (e.g. Swedish National TV show "Babel", Polish National News, BBC 2 Countryfile, BBC News), and many newspaper articles about bees and insect declines. For example, a paper on which I was author (Hallmann et al. 2017) on insect declines in Germany was the most discussed paper in the UK in 2017 (across all disciplines), and was ranked 6th amongst the most discussed papers in the world. Environment Secretary Michael Gove announced a U-turn in government policy on further restrictions on neonicotinoid insecticides, citing this study as one reason for his change of heart.
Year(s) Of Engagement Activity 2014,2015,2016,2017,2018
 
Description Numerous public talks to e.g. beekeepers, natural history societies, schools, literature festivals. Approximately 50 per year 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact In total several thousand people have heard me give talks on bumblebee ecology and conservation, and on the impacts of pesticides on bees.

I have numerous further invites to give talks
Year(s) Of Engagement Activity Pre-2006,2006,2007,2008,
 
Description Popular Science Books 
Form Of Engagement Activity A magazine, newsletter or online publication
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact I have published three popular science books, A Sting in the Tale (2013), A Buzz in the Meadow (2014), and Bee Quest (2017). Together they have so far sold >160,000 copiues, and been translated into 14 languages.
Year(s) Of Engagement Activity 2013,2014,2015,2016,2017
 
Description Talks on bees and related issues on YouTube 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Several of my talks on bee ecology and conservation, and on impacts of pesticides, are available on Youtube and have been watched many thousands of times. I also have a Youtube channel which has various short videos on bee-related matters, focussed on encouraging the public to plant flowers for them, and create nest sites for them. These videos have, collectively, been viewed >69,000 times
Year(s) Of Engagement Activity 2014,2015,2016,2017,2018
URL https://www.youtube.com/channel/UCbnBys2Hl1T26dzO_nbgbiw?view_as=subscriber
 
Description The Buzz Club 
Form Of Engagement Activity Engagement focused website, blog or social media channel
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Public/other audiences
Results and Impact We have set up a citizen-science organisation, The Buzz Club, to monitor pollinator numbers and engage the public in learning about bees and other pollinators. Over 2,000 people have taken part in our activities to date, and 140 are now paying members of the club.
Year(s) Of Engagement Activity 2014,2015,2016,2017,2018
URL http://www.thebuzzclub.uk