Specific floral resources may help bees to face environmental challenges such as parasite infection, as recently shown for sunflower pollen. Whereas this pollen diet is known to be unsuitable for the larval development of bumble bees, it has been shown to reduce the load of a trypanosomatid parasite (Crithidia bombi) in the bumble bee gut. Recent studies suggested it could be due to phenolamides, a group of compounds commonly found in flowering plants. We, therefore, decided to assess separately the impacts of sunflower pollen and its phenolamides on a bumble bee and its gut parasite. We fed Crithidia-infected and -uninfected microcolonies of Bombus terrestris either with a diet of willow pollen (control), a diet of sunflower pollen (natural diet) or a diet of willow pollen supplemented with sunflower phenolamides (supplemented diet). We measured several parameters at both microcolony (i.e., food collection, parasite load, brood development and stress responses) and individual (i.e., fat body content and phenotypic variation) levels. As expected, the natural diet had detrimental effects on bumble bees but surprisingly, we did not observe any reduction in parasite load, probably because of bee species-specific outcomes. The supplemented diet also induced detrimental effects but by contrast to our a priori hypothesis, it led to an increase in parasite load in infected microcolonies. We hypothesised that it could be due to physiological distress or gut microbiota alteration induced by phenolamide bioactivities. We further challenged the definition of medicinal effects and questioned the way to assess them in controlled conditions, underlining the necessity to clearly define the experimental framework in this research field.

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.

Bumble bees are important pollinators for many temperate crops. Because of the growing demand for food from entomophilous crops, bumble bee colonies are commercially reared and placed in fields or greenhouses to guarantee sufficient pollination services. Besides, commercial colonies are increasingly used in laboratories for various bioassays under controlled conditions. For both usages, bumble bee colonies are commonly provided with sugar solution and honey bee-collected pollen pellets. However, the latter display several disadvantages since they may contain pollutants, pathogens, or toxic phytochemicals. Consequently, companies have developed pollen-free artificial diets to sustain colonies. Such diets are designed to boost worker health in the field, in complement of floral pollen collected by workers outside the colonies, but their suitability in ‘closed’ systems without access to floral pollen, such as in laboratory bioassays, is arguable. Here, we used microcolonies of the commercially important bumble bee Bombus terrestris L. (Hymenoptera: Apidae) to assess the suitability of five artificial pollen substitutes and three mixed diets. We also assessed the evaporation rate of the different diets as it could impact their suitability. At the end of the bioassays, microcolonies fed the artificial diets showed a reduced offspring development when compared to microcolonies fed natural pollen, which was partly offset by mixing these diets with natural pollen. By contrast, the artificial diets did not have deleterious effects on worker’s health. We discuss the potential nutritional and physical causes of artificial diets unsuitability for offspring development and encourage further research to accordingly establish appropriate pollen-free diets for bumble bee breeding.

Bumblebees (Apidae: Bombus spp.) are a major group of wild and domesticated bees that provide crucial ecosystem services through wildflower and crop pollination. However, most of bee populations, including bumblebees, are declining worldwide, partly because of parasite spill-over and spill-back between bumblebee commercial colonies and wild populations. Breeders have to cope with invasions by a vast array of bumblebees’ parasites, and techniques need to be developed to prevent such invasions to support breeders and wild bee populations. Our 10-year study is based on 327 nests of seven bumblebee species (B. humilis, B. hypnorum, B. lapidarius, B. lucorum, B. pascuorum, B. sylvarum, B. terrestris) reared in outdoor boxes. Some boxes were equipped with parasite-preventing techniques, namely (i) an airlock (n = 2) or (ii) an additional chamber with natural fragrances (n = 74). We recorded the invasion of the nests by the wax moth Aphomia sociella, the eulophid Melittobia acasta and the cuckoo bumblebees Bombus subgenus Psithyrus spp. Overall, 8.26 %, 1.53 % and 3.67 % of the colonies were invaded by A. sociella, M. acasta and Psithyrus spp., respectively, without coinfection. Neither the airlock nor the additional chamber with natural fragrances prevented A. sociella infestation. Despite that no nest equipped with an airlock or an additional chamber with natural fragrances was invaded by M. acasta or Psithyrus spp., we lacked replicates to properly demonstrate the efficiency of these techniques. Nest inspection remains a time-consuming but powerful technique to reduce artificial nest spoilage by parasites, yet it is inefficient against tiny invaders (< 1 mm) that are left unnoticed. We therefore encourage further studies to actively seek for parasite-preventing techniques to reduce artificial nest spoilage and to mitigate spill-over towards wild populations.

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