Stressful environments put bumblebees at risk

This blog post is provided by Cristina Botías and Dave Goulson and tells the #StoryBehindThePaper for the article “Multiple stressors interact to impair the performance of bumblebee (Bombus terrestris) colonies”.

Cristina Botías is a Research Fellow at the Apicultural and Agri-environmental Research Center (CIAPA-IRIAF, Spain), working on a range of applied research related to bee health. Dave Goulson is a Professor of Biology at the University of Sussex (UK), specializing in the ecology and conservation of bumblebees and other insects. He is author of a number of popular science books, including A Sting in the Tale, and The Garden Jungle.
Bumblebee (Bombus terrestris) foraging in a bramble flower. Photo: Dave Goulson

The causes underlying the ongoing decline of bumblebees have been much debated, and include habitat loss, pesticides, emerging diseases, climate change and probably others too. The large majority of scientific studies to date have tended to focus on one stressor at a time, yet we know that bumblebees are very likely to be simultaneously exposed to multiple stressors. For example, bees foraging in both farmland and gardens are frequently exposed to mixtures of pesticides contained in pollen and nectar of crops, ornamental, and wild flowers, and we have previously found that bumblebees can contain up to seven different pesticides in their body tissues. Bees are also impacted by a diversity of native and emerging pathogens, the latter including one suspected to seriously affect their health, the microsporidium Nosema ceranae, which infects gut epithelia of adult bees. Few previous studies have attempted to examine the complex interacting effects of exposure to multiple stressors.

In a recent paper in the Journal of Animal Ecology we evaluated how combined effects of four common environmental stressors, the neonicotinoid thiamethoxam, the pyrethroid cypermethrin, the EBI-fungicide tebuconazole and the gut parasite N. ceranae, interact to affect bumblebees at the individual and colony levels. We established seven treatment groups of colonies that we exposed to different combinations of these stressors for two weeks under laboratory conditions.

Bumblebees colonies were kept in laboratory conditions (25° C, 50-60% relative humidity) for two weeks where they were exposed to pesticides via the pollen and sugar syrup solution provided according to their treatment group. Pesticide-spiked food was provided to the relevant treatments in one of the two pollen/nectar feeder (‘pesticide feeder’), and pesticide-free food in the other pollen/nectar feeder (‘uncontaminated feeder’). Photo: Cristina Botías

Colonies were subsequently placed in the field for seven weeks to evaluate the effect of treatments on various measures of bee health. These included the prevalence of N. ceranae, expression levels of immunity and detoxification-related genes, food collection, colony weight gain, worker and male numbers, and production of worker brood and reproductives.

We found that exposure to pesticide mixtures reduced food collection by bumblebees.  Furthermore, all immunity-related genes were upregulated in the bumblebees inoculated with N. ceranae when they had not been exposed to pesticides, indicating that pesticide mixtures may interfere with the transcription of some genes encoding defense mechanisms to pathogen challenge. Previous research showed that exposure to neonicotinoid insecticides leads to immuno-suppression in honeybees, which in turn promotes the replication of pathogens in insects with covert infections. In our study, we did not find a correlation between exposure to the neonicotinoid thiamethoxam, and the prevalence of N. ceranae, but, intriguingly, exposure to both the fungicide and the pyrethroid led to lower prevalence of this pathogen. There are clearly interactions between pesticide exposure and parasites that we do not yet understand.

The field site was situated in an orchard at Stanmer Organics (Brighton, East Sussex, UK), which has been Soil Association certified organic for the past 10 years and is located within Stanmer Park Local Natural Reserve (about 5,000 ha of open and wooded land). Colonies were randomly and evenly distributed across the orchard in shaded positions, leaving at least 5 m separation. Photo: Cristina Botías

At the colony level, combined exposure to the three-pesticide mixture and N. ceranae reduced bumblebee colony growth, and all treatments had detrimental effects on brood production compared to controls. More significantly, colonies exposed to the neonicotinoid insecticide produced 40-76% fewer queens than control colonies. Bumblebees, like solitary bees, have an annual lifecycle whereby reproductive females (queens) initiate a colony in the spring. The success of a colony can be measured in the number of reproductives (i.e. males and queens) produced at the end of the season, as only they will contribute to initiating new colonies in the following spring. Therefore, the large reduction in queens in the colonies exposed to mixtures containing neonicotinoid insecticides may lead to serious effects on bumblebee population dynamics.

Overall, our findings show that exposure to combinations of stressors that bumblebees frequently come into contact with has detrimental effects on colony health and performance and could therefore have an impact at the population level. These results are worrying since the variety of chemical, physical, and biological stressors associated with global change that represent potential environmental hazards to pollinators, such as bumblebees, has increased rapidly in recent years. Understanding the interactions between different stressors will be crucial for improving our ability to mitigate pressures on wild bee populations and ensure pollination services for crops and wildflowers into the future.

Our study shows that is it possible to study multiple stressors (four in our case), and contributes to better understanding of the responses of animals to field-relevant combinations of stressors, a pressing topic in the field of animal ecology today. It also has significant implications for current practices and policies for pesticide risk assessment, which focus exclusively on evaluating the impact of exposing otherwise healthy bees to one pesticide at a time. This is a poor representation of the real world where bees (and other organisms) are likely to encounter pesticides in combination and while simultaneously attempting to cope with other stressors.

Read the paper:

Read the full paper: Botías, C, Jones, JC, Pamminger, T, Bartomeus, I, Hughes, WOH, Goulson, D. Multiple stressors interact to impair the performance of bumblebee Bombus terrestris colonies. J Anim Ecol. 2020; 00: 1– 17.

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