Multiple stressors interact to impair the performance of bumblebee Bombus terrestris colonies

Abstract

Bumblebees are constantly exposed to a wide range of biotic and abiotic stresses which they must defend themselves against to survive. Pathogens and pesticides represent important stressors that influence bumblebee health, both when acting alone or in combination. To better understand bumblebee health, we need to investigate how these factors interact, yet experimental studies to date generally focus on only one or two stressors. The aim of this study is to evaluate how combined effects of four important stressors (the gut parasite Nosema ceranae, the neonicotinoid insecticide thiamethoxam, the pyrethroid insecticide cypermethrin and the EBI fungicide tebuconazole) interact to affect bumblebees at the individual and colony levels. We established seven treatment groups of colonies that we pulse exposed to different combinations of these stressors for 2 weeks under laboratory conditions. Colonies were subsequently placed in the field for 7 weeks to evaluate the effect of treatments on the prevalence of N. ceranae in inoculated bumblebees, expression levels of immunity and detoxification‐related genes, food collection, weight gain, worker and male numbers, and production of worker brood and reproductives. Exposure to pesticide mixtures reduced food collection by bumblebees. All immunity‐related genes were upregulated in the bumblebees inoculated with N. ceranae when they had not been exposed to pesticide mixtures, and bumblebees exposed to the fungicide and the pyrethroid were less likely to have N. ceranae. Combined exposure to the three‐pesticide mixture and N. ceranae reduced bumblebee colony growth, and all treatments had detrimental effects on brood production. The groups exposed to the neonicotinoid insecticide produced 40%–76% fewer queens than control colonies. Our findings show that exposure to combinations of stressors that bumblebees frequently come into contact with have detrimental effects on colony health and performance and could therefore have an impact at the population level. These results also have significant implications for current practices and policies for pesticide risk assessment and use as the combinations tested here are frequently applied simultaneously in the field. Understanding the interactions between different stressors will be crucial for improving our ability to manage bee populations and for ensuring pollination services into the future.

Landscape Enhancements in Apple Orchards: Higher Bumble Bee Queen Species Richness, but No Effect on Apple Quality

“…Despite the growing body of evidence documenting negative impacts of pesticides on bumble bees [ 26 , 76 , 77 , 78 , 79 ], and contrary to one of our hypotheses, we found a negative effect of intensity of pesticide use on the site occupancy by bumble bee queens for only one of the eight (groups of) species we detected in orchards, namely, B. ternarius ( Figure 4 C). Aside from the fact that B. ternarius was the third most captured species in our study ( Figure 3 ) and that this may have led to an improved capacity of detecting such an effect, it remains that this result may also stem from interspecific differences in exposure or sensitivity to pesticides.…”

“…As expected, species richness was negatively influenced by the intensity of pesticide use. As mentioned above and shown here, evidence of negative effects of pesticides on bumble bee species, such as B. impatiens and B. terrestris, is mounting [ 26 , 76 , 77 , 78 , 79 ]. However, studies looking at the effects of pesticides on bee communities remain scarce, and those that did so while controlling for imperfect species detection are even scarcer.…”

“…In 2019, 17 pesticides, including five neonicotinoids and four fungicides, were detected in 379 apple juice samples evaluated by the Pesticide Data Program (PDP) [ 22 ]. Such combinations of pesticides are well known to be detrimental to bees [ 21 , 23 , 24 , 25 , 26 ]. For example, the fungicide imazalil, when used in mixture with common insecticides (namely: fipronil, thiamethoxam and cypermethrin), synergized the insecticidal toxicity on bumble bees [ 21 ].…”

The gut parasiteNosema ceranaeimpairs olfactory learning in bumblebees

“…Ingestion of N. ceranae spores exerts a stress that can reduce cognition. N. ceranae is known to alter the immune system of bees by increasing oxidative responses (Kurze et al, 2016) or modulating the expression of antimicrobial peptides (Antúnez et al, 2009; Botías et al, 2020; Sinpoo, 2018). Stimulation of the immune system of bees with non-pathogenic elicitors, as lipopolysaccharides (LPS), was shown to reduce learning abilities in honey bees, that were less able to associate an odour with a reward (Mallon et al, 2003), and bumblebees, that showed lower performances in odour (Mobley and Gegear, 2018) and colour differential learning tasks (Alghamdi et al, 2008; Mobley and Gegear, 2018).…”

Environmental differences explain subtle yet detectable genetic structure in a widespread pollinator

“…It is The copyright holder for this preprint this version posted July 10, 2021. ; https://doi.org/10.1101/2021.07.09.451741 doi: bioRxiv preprint the spatial arrangement of plant species producing nectar or pollen in high quantities (59,79,80) on structuring bumble bee populations. Finally, habitat alterations such as intensified farming practices might also structure populations, in particular through a synergy with natural stressors (81,82).…”