Generalized host‐plant feeding can hide sterol‐specialized foraging behaviors in bee–plant interactions

Abstract

Host-plant selection is a key factor driving the ecology and evolution of insects.While the majority of phytophagous insects is highly host specific, generalist behavior is quite widespread among bees and presumably involves physiological adaptations that remain largely unexplored. However, floral visitation patterns suggest that generalist bees do not forage randomly on all available resources. While resource availability and accessibility as well as nectar composition have been widely explored, pollen chemistry could also have an impact on the range of suitable host-plants. This study focuses on particular pollen nutrients that cannot be synthesized de novo by insects but are key compounds of cell membranes and the precursor for molting process: the sterols. We compared the sterol composition of pollen from the main hostplants of three generalist bees: Anthophora plumipes, Colletes cunicularius, and Osmia cornuta, as well as one specialist bee Andrena vaga. We also analyzed the sterols of their brood cell provisions, the tissues of larvae and nonemerged females to determine which sterols are used by the different species. Our results show that sterols are not used accordingly to foraging strategy: Both the specialist species A. vaga and the generalist species C. cunicularius might metabolize a rare C 27 sterol, while the two generalist species A. plumipes and O. cornuta might rather use a very common C 28 sterol. Our results suggest that shared sterolic compounds among plant species could facilitate the exploitation of multiple host-plants by A. plumipes and O. cornuta whereas the generalist C. cunicularius might be more constrained due to its physiological requirements of a more uncommon dietary sterol. Our findings suggest that a bee displaying a generalist foraging behavior may sometimes hide a sterol-specialized species. This evidence challenges the hypothesis that all generalist free-living bee species are all able to develop on a wide range of different pollen types. K E Y W O R D Sbee-flower interactions, generalization, insects, physiological constraints, sterols | 151 VANDERPLANCK Et AL.

Pollen sterols are associated with phylogenetics and environment but not with pollinators

“…For example, Standifer et al (1968) suggested a lack of phylogenetic constraints of pollen sterol composition based on the evidence of large variation in three Salicaceae species. Vanderplanck et al (2020a), in contrast, found similar pollen sterol composition within the genus Salix and our interpretation of the data published by Villette et al (2015) suggested the occurrence of some pollen sterols was phylogenetically constrained. Since most studies focused on a few plant species, they were insufficient to reach a general overview of the patterns of pollen sterol diversity across plant taxa and their drivers.…”

“…This suggests an overall trade-off of these two groups, the balance of which may be governed by DWF1 (sterol-Δ 24 -reductase) activity. Data from previous studies (Villette et al, 2015;Vanderplanck et al, 2020a) The composition of phytosterols appears to be tissue-dependent (Nes, 1990;Nes et al, 1993). For example, 24-methylenecholesterol has been identified as the main pollen sterol in many Cactaceae (Fig.…”

“…Honeybees, for example, require 24-methylenecholesterol (Herbert et al 1980;Chakrabati et al, 2020) so must collect pollen from plant species that produce this sterol to rear brood. Bee sterols are similar to those occurring in the pollen on which they feed (Vanderplanck et al, 2020a) but differ across bee taxa suggesting bees are what they eat with respect to sterols. Wild pollinators range from pollen generalists to specialists (Rasmussen et al, 2020) and for some species, this specialism may be mediated by pollen sterols.…”

“…Phytosterols are a class of lipids with key metabolic and ecological functions for plants (Nes & McKean, 1977; Vanderplanck et al ., 2020a). For example, they regulate membrane fluidity and permeability (Grunwald, 1971; Schuler et al ., 1991; Hartmann, 1998), and act as precursors for metabolic signals such as brassinosteroid growth hormones (Grove et al ., 1979; Chung et al ., 2010) that promote cell division, and mediate reproduction in plants and protect them against environmental stresses (Khripach et al ., 2000).…”

Pollen Protein: Lipid Macronutrient Ratios May Guide Broad Patterns of Bee Species Floral Preferences

“…Higher pollen sterol levels have been repeatedly linked to bumble bee colony health and fitness [24,25]. Dietary needs based on the composition of lipid and sterol nutrients are likely to be species-specific; different bee taxa show characteristic body-lipid composition likely derived from their pollen diet [46], and lipid preference may guide host-plant choice for specialists and generalists alike [47]. The overconsumption of diets too high in lipid content can be detrimental to bumble bee health and possibly lead to their avoidance [8,43].…”