To bee or not to bee: The ‘raison d'être’ of toxic secondary compounds in the pollen of Boraginaceae

Abstract

While the presence of secondary compounds in floral nectar has received considerable attention, much less is known about the ecological significance and evolutionary origin of secondary ‘toxic’ compounds in pollen. It is unclear whether the presence of these compounds in pollen is non‐adaptive and due to physiological ‘spillover’ from other floral tissues, or whether these compounds serve an adaptive function related to plant–pollinator interactions, such as protection of pollen against pollen thieves. Combining an experimental approach with phylogenetic comparative methods, and using western Palaearctic Boraginaceae as a model system, we investigate how pollen secondary metabolites influence, and are influenced by, relationships with bees, the main functional group of pollen‐foraging pollinators. We found a significant relationship between the levels of secondary compounds in the corollas and those in the pollen in the investigated species of Boraginaceae, suggesting that baseline levels of pollen secondary compounds may partly be due to spillover from floral tissues. At realistic levels, pollen secondary compounds showed significant detrimental effects on bee pre‐imaginal development, in agreement with previous egg‐transfer experiments showing that in some cases Boraginaceae pollen did not support pre‐imaginal development in bees not specialized on these plants. We also show that phylogenetically independent Boraginaceae taxa rewarding pollinators with pollen in addition to nectar exhibit significantly lower levels of toxic compounds in the pollen than taxa where the main reward is postulated to be nectar. Lastly, in contrast to our predictions, there was no positive association between toxin levels in the pollen of a given plant taxon and the number of bee species specialized on this taxon. We integrate all these findings and formulate an evolutionary scenario to account for the presence of toxic compounds in the pollen of Boraginaceae. We suggest that baseline levels of toxic compounds may be found in pollen due to spillover from other floral tissues and not primarily because of bee–flower interactions. Since pollen toxins can have detrimental effects on bees, we propose that selection acts to lower pollen toxin levels in plants where pollen, in addition to nectar, serves as a reward to bees. A free Plain Language Summary can be found within the Supporting Information of this article.

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

“…Such "filtering" mechanisms allow for interactions with the most efficient pollinators to be maximized, while minimizing pollen loss due to excessive harvesting by pollen-feeding visitors (Müller, 1996). In the absence of specialized flower morphology, such "filtering" may occur through chemical properties of pollen, for instance occurrence of specialized metabolites that render the resource unsuitable to some bee species (i.e., fitness loss caused by pollen consumption) (Praz et al, 2008b;Trunz et al, 2020;Vanderplanck et al, 2020). In order to be an effective defense mechanism, these specialized metabolites have compulsorily to generate an avoidance behavior in bees (i.e., floral visits without pollen consumption), which then ensures the availability of pollen for plant reproduction.…”

“…The presence of a given specialized metabolite at a given concentration in nectar or in pollen may then influence the detection ability of bees, as well as their foraging decision. This hypothesis is strengthened by the ecological "raison d'être" of specialized metabolites from the plant perspective: while a phagostimulatory activity of nectar through the occurrence of specialized metabolites might attract more specialized pollinators and subsequently enhance the plant fitness, a phagostimulatory activity of pollen would have a reverse effect by compromising the plant's reproductive success (e.g., Gosselin et al, 2013;Trunz et al, 2020). This highlights the importance for investigating not only the nectar specialized metabolites but also the pollen ones using appropriate and biologically relevant experimental designs.…”

Individual-level specialisation and interspecific resource partitioning in bees revealed by pollen DNA metabarcoding

“…An interesting fact is that pollen of Echium vulgare was the dominant source of pollen for all three Ceratina species, based on the proportion of sequencing reads. The pollen of E. vulgare has a very high protein content (35% crude protein in the dry matter according to Somerville and Nicol (2006)), which makes it a potentially excellent resource for bees, but it contains high concentrations of pyrrolizidine alkaloids (Boppré et al, 2008;Lucchetti et al, 2016;Trunz et al, 2020) toxic to insects (Narberhaus et al, 2005;Macel, 2011). Only a restricted range of solitary bee species can successfully develop on the pollen of E. vulgare (Praz et al, 2008;Sedivy et al, 2011;Trunz et al, 2020).…”

“…Only a restricted range of solitary bee species can successfully develop on the pollen of E. vulgare (Praz et al, 2008;Sedivy et al, 2011;Trunz et al, 2020). In particular, some species of the genus Hoplitis (Hymenoptera: Megachilidae) are specialised on Echium and other plants in the family Boraginaceae (Sedivy et al, 2013), which are also known to contain pyrrolizidine alkaloids (El-Shazly et al, 1998;El-Shazly and Wink, 2014;Trunz et al, 2020). Our results suggest that the three species of Ceratina we studied also have physiological adaptations to develop on the pollen of E. vulgare, which allows them to utilise its protein-rich pollen Somerville and Nicol (2006).…”

“…The pollen of E. vulgare has a very high protein content (35% crude protein in the dry matter according to Somerville and Nicol (2006)), which makes it a potentially excellent resource for bees, but it contains high concentrations of pyrrolizidine alkaloids (Boppré et al, 2008;Lucchetti et al, 2016;Trunz et al, 2020) toxic to insects (Narberhaus et al, 2005;Macel, 2011). Only a restricted range of solitary bee species can successfully develop on the pollen of E. vulgare (Praz et al, 2008;Sedivy et al, 2011;Trunz et al, 2020). In particular, some species of the genus Hoplitis (Hymenoptera: Megachilidae) are specialised on Echium and other plants in the family Boraginaceae (Sedivy et al, 2013), which are also known to contain pyrrolizidine alkaloids (El-Shazly et al, 1998;El-Shazly and Wink, 2014;Trunz et al, 2020).…”