Queens under pressure -  do pesticides provide additional challenges for bumblebees starting a colony?

The determined buzzing of queen bumblebees after a long winter is a timely reminder that spring is on its way. They industriously search for pollen and nectar to refuel after a lengthy hibernation, and find nesting sites to start their new colony. The survival and health of these queens is essential to the bumblebee life-cycle.
Queens under pressure -  do pesticides provide additional challenges for bumblebees starting a colony?

The paper in Nature Ecology & Evolution is here: http://go.nature.com/2j8sHgU

As Frederick Sladen observed in his book ‘The Humble-Bee’ in 1912; ‘The story of the life of the humble-bee is largely that of the queen. From start to finish she is the central and dominating personage upon whose genius and energy the existence of the race depends. For she alone survives the winter, and, unaided, founds the colony in which she takes the position of its most important member.’

Bumblebee queen foraging on oilseed rape (photo: Emily Bailes)

Bumblebee queen foraging on oilseed rape (photo: Emily Bailes)

Queens are faced with many potential dangers along the way. Already weakened by months of hibernation without food, they are at risk from parasites, predation, and a lack of flowers from which to feed. And the food they do find may not be all that it seems – there is considerable evidence that pollen and nectar from both crop flowers, such as oilseed rape, as well as wild flowers growing in agricultural areas, are often contaminated with a cocktail of chemicals which are applied to protect crops from pests. Much research has been done into the impacts of these pesticides on bees – particularly honeybees. However, the impacts on queen bumblebees, which could have important consequences for the future of their colonies, are largely unknown. 

During my PhD I worked with Professors Mark Brown and Nigel Raine and their groups at Royal Holloway University of London, giving me access to a wealth of expertise in the fields of bumblebee ecology, parasitology, and behaviour. Observations from field work indicated that queens of several bumblebee species will forage in and around mass-flowering crops such as oil seed rape in the spring. We had many questions about how pesticides and various other interacting stressors might have impacts upon queen bumblebees and their ability to establish a colony in the spring. Do pesticides have an impact on bumblebee queens at doses they may encounter in the field? Does exposure have a greater impact when queens are additionally challenged with a parasite infection (as is often the case in the wild)?

Testing these questions with a field trial would be desirable in many ways, however, keeping track of hibernating and emerging queens, whilst controlling for variation in their environment would be impossible. We were therefore faced with the challenge of how to re-create these scenarios in the lab. Firstly, newly emerged Bombus terrestris reproductive females (gynes) needed to be paired up to mate, and so were introduced to a selection of eligible (and unrelated) males in a custom built ‘mating cage’. Once the males had completed their task, the queens were exposed to a common and prevalent parasite called Crithidia bombi. This tiny microscopic trypanosome lives and reproduces in the gut of bumblebees, and is passed on through infected faeces on flowers and within colonies. Having consumed a full dose of Crithidia, the queens were carefully packed into sand-filled tubes and refrigerated at 4 ˚C. This was done to mimic hibernation, when queens will burrow into soft earth in north facing banks to wait out the winter months.

After a 6 or 12 week hibernation, more than 200 queens were set up in individual boxes with a ball of pollen to encourage egg-laying. The bee room (which was our home for the next 13 weeks) is a small, red-lit, temperature controlled room, with rows of queen boxes lined up on shelves. In here, queens were provided with a syrup solution either containing the insecticide thiamethoxam (a neonicotinoid used globally as a seed treatment for crops such as oil seed rape), or with a control solution. Each day would start with a check of the queens to record and remove dead individuals, to look for signs of egg-laying (the queens lay eggs into the pollen ball and cover it with wax), and to replenish food. In order to test for parasite infection, I checked samples of faeces (bumblebees will conveniently provide a sample as a defensive response to disturbance), and was able to confirm infection in the majority of queens which had been exposed to Crithidia.

Bumblebee (Bombus terrestris) queens trying to establish colonies in the Royal Holloway bee room after hibernation (photo: Judit Bagi)

Bumblebee (Bombus terrestris) queens trying to establish colonies in the Royal Holloway bee room after hibernation (photo: Judit Bagi)

Of the 231 queens in the experiment, 197 survived through to 10 weeks, and of these, 89 initiated a colony. Both exposure to pesticide and duration of hibernation resulted in differences in the numbers of queens starting a colony. Queens exposed to thiamethoxam were 26% less likely to lay eggs, whilst a short hibernation resulted in queens being 55% less likely to lay eggs compared to a longer hibernation. We found no impacts of Crithidia infection on the ability of queens to start a colony in this study.

The difference observed between queens that underwent long and short hibernation durations in our experiment might be expected – although queens hibernating for longer lost more body mass, this species has evolved to hibernate for much longer periods (6 months or more) in the wild, and presumably derive benefits from this. The reduction in egg laying shown by the pesticide exposed group was marked, and could have serious impacts for bumblebee queens foraging in agricultural environments. Interestingly, the thiamethoxam treated queens which did lay eggs, tended to start doing so earlier than their control group counterparts. The reason for this shift in timing, and its potential knock-on impacts for queens in the wild are not yet understood. Perhaps, like many other organisms, bumblebees are able to shift the timing of their reproductive effort in response to physiological stress. Whether this would be an advantage or a disadvantage in the wild, where an early colony may benefit from early access to resources, or conversely may be put out of synch with the flowering of key forage plants, is as yet unknown.  

Bumblebee (Bombus terrestris) queen incubating her eggs on a pollen ball in the bee room (photo: Judit Bagi)

Bumblebee (Bombus terrestris) queen incubating her eggs on a pollen ball in the bee room (photo: Judit Bagi)

We were keen to explore the potential impacts of our findings at a population level, and our co-author Professor Vincent Jansen, was able to use computer modelling to investigate this further. By using our empirical results, combined with published data on hibernation survival, colony initiation and new queen production, along with estimates for queen nest finding and mating success in the field (empirical data is not currently available for these), he found that a reduction in colony founding by queens exposed to thiamethoxam is likely to carry a substantially increased risk of population extinction.  

Our findings show that even at field relevant levels, thiamethoxam exposure can have considerable impacts on bumblebee queens, and potentially on bumblebee populations. These results contribute to a growing body of evidence that certain pesticides are putting additional pressure on a group of important pollinators already faced with the widespread loss of their key habitats, infection with parasites and pathogens, and competition from invasive species. Policy and legislation on plant protection products needs to reflect this, and particularly to take into account the complex and varied life-history of the many species at risk of exposure.

Baron, Gemma L., V. A. A. Jansen, M. J. F. Brown, and N. E. Raine (2017). Pesticide reduces bumblebee colony establishment and increases probability of population extinction. Nature Ecology & Evolution 1: 1308-1316. doi:10.1038/s41559-017-0260-1

Baron, G. L., N. E. Raine and M. J. F. Brown (2017). General and species-specific impacts of a neonicotinoid insecticide on the ovary development and feeding of wild bumblebee queens. Proceedings of the Royal Society B-Biological Sciences 284: 20170123. doi:10.1098/rspb.2017.0123


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