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

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.

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.

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.