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

Abstract

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.

Mouthparts of the bumblebee (Bombus terrestris)exhibit poor acuity for the detection of pesticides in nectar

“…For this reason, it is likely that nectar palatability is largely determined by the sensilla on the proboscis. Based on our current results and those of previous studies (Sculfort et al, 2021; Tiedeken et al, 2014), we predict that bumblebees have a limited ability to detect naturally-occurring concentrations of toxic or bitter compounds in nectar. Future studies that survey a greater variety of compounds will be necessary to confirm this.…”

Fertilizer and herbicide alter nectar and pollen quality with consequences for pollinator floral choices

“…It will be important to test the fitness implications of this variance in floral resource quality for pollinating insects, especially as their preferences do not always increase their fitness ( Hoover et al, 2012 ). Our study did not evaluate other components of pollen and nectar, such as bacteria, sterols, plant secondary metabolites, and micro-nutrients, but they have shown to be important drivers of both flower-visiting insect behaviour and fitness ( Palmer-Young et al, 2018 ; Vannette, 2020 ; Sculfort et al, 2021 ; Filipiak et al, 2022 ).…”

Seed treatment with clothianidin induces changes in plant metabolism and alters pollinator foraging preferences

“…Knauer and Schiestl ( 2017 ) found that B. napa plants that had increased levels of the glucosinolate Glucobrassicanapin caused by foliar herbivory tended to have reduced visitation by bumblebees, but this effect could also have been related to indirect effects such as delayed flowering or a change in volatile organic compounds (discussed below). To our knowledge, the only available test whether glucosinolates have a direct effect on foraging preference of bees was conducted by testing consumption of sugar solutions containing different concentrations of the glucosinolates Scopolamine, Amygdalin and Sinigrin by bumblebees (Sculfort et al 2021 ). However, results were difficult to interpret, because both high and low but not intermediate concentrations of Amygdalin and Sinigrin repelled bees, whereas Scopolamine only had attractant effects (Sculfort et al 2021 ).…”

“…To our knowledge, the only available test whether glucosinolates have a direct effect on foraging preference of bees was conducted by testing consumption of sugar solutions containing different concentrations of the glucosinolates Scopolamine, Amygdalin and Sinigrin by bumblebees (Sculfort et al 2021 ). However, results were difficult to interpret, because both high and low but not intermediate concentrations of Amygdalin and Sinigrin repelled bees, whereas Scopolamine only had attractant effects (Sculfort et al 2021 ). In addition we cannot exclude that additonal plant parameters not measured by us could be the causative agent.…”

“…Glucosinolates are defense compounds, also called mustard oils, that normally increase as well as allocate in all plant tissues when Brassicaceae are attacked by herbivores or pathogens (Fahey et al 2001 ) and are enzymatically hydrolyzed into toxic break-down products upon plant tissue damage, where they repel or kill many herbivores that come into contact with them (Bones and Rossiter 1996 ). Glucosinolates can be attractive to some insect herbivores specialized on Brassicaceae, but can also repel insects (Hopkins et al 2009 ), including bumblebees (Sculfort et al 2021 ). As a result, plant defense induced by neonicotinoids could also impact the attractiveness of Brassicaceae plants to pollinators.…”