Specialized Metabolites in Floral Resources: Effects and Detection in Buff-Tailed Bumblebees

The selection of appropriate food resources by bees is a critical aspect for the maintenance of their populations, especially in the current context of global change and pollinator decline. Wild bees have a sophisticated ability to forage selectively on specific resources, and can assess the quality of pollen using contact chemosensory perception (taste). While numerous studies have investigated the detection of pollen macronutrients in bees and their impact on bee health and reproductive success, only a few studies have described the gustatory responses of bees toward specialized metabolites. In addition, these studies mostly focused on the response to nectar and neglected pollen, which is the main food resource for both bee imagines and larvae. Whether bees have the ability to detect specialized toxic metabolites in pollen and then rapidly adapt their foraging behavior to avoid them is very little studied. In this study, we tested whether pollen specialized metabolites affect bumblebees at both the micro-colony and individual levels (i.e., bioassays using supplemented pollen), and whether foragers detect these specialized metabolites and potentially display an avoidance behavior (i.e., preference tests using supplemented syrup). Bumblebees were fed with either amygdalin-, scopolamine- or sinigrin-supplemented pollen diets in ratios that mimic 50%, 100%, and 200% of naturally occurring concentrations. We found no effect of these specialized metabolites on resource collection, reproductive success and stress response at the micro-colony level. At the individual level, bumblebees fed on 50%-amygdalin or 50%-scopolamine diets displayed the highest scores for damage to their digestive systems. Interestingly, during the preference tests, the solution with 50%-scopolamine displayed a phagostimulatory activity, whereas solution with 50%-amygdalin had a deterrent effect and could trigger an active avoidance behavior in bumblebees, with a faster proboscis retraction. Our results suggest that regulation of toxin intake is not as well-established and effective as the regulation of nutrient intake in bees. Bees are therefore not equally adapted to all specialized pollen metabolites that they can come into contact with.