Sub-lethal but potentially devastating - The novel insecticide flupyradifurone impairs collective brood care in bumblebees.

The worldwide decline in pollinating insects is alarming. One of the main anthropogenic drivers is the massive use of pesticides in agriculture. Risk assessment procedures test pesticides for mortality rates of well-fed, parasite free individuals of a few non-target species. Sublethal and synergistic effects of co-occurring stressors are usually not addressed. Here, we present a simple, wildly applicable bio-essay to assess such effects. Using brood thermoregulation in bumblebee microcolonies as readout, we investigate how this collective ability is affected by long-term feeding exposure to the herbicide glyphosate (5 mg/l), the insecticide flupyradifurone (0.4 mg/l) and the combination of both, when co-occurring with the natural stressor of resource limitation. Documenting brood temperature and development in 53 microcolonies we find no significant effect of glyphosate, while flupyradifurone significantly impaired the collective ability to maintain the necessary brood temperatures, resulting in prolonged developmental times and a decrease in colony growth by over 50 %. This reduction in colony growth has the potential to significantly curtail the reproductive chances of colonies in the field. Our findings highlight the potentially devastating consequences of flupyradifurone use in agriculture even at sub-lethal doses and underline the urgent need for improved risk assessment procedures.