Behavioural and molecular responses to pesticide exposure in bumblebees.

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.

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.