Solitary bee larvae prioritize carbohydrate over protein in parentally provided pollen

Abstract

Most organisms must regulate their nutritional intake in an environment full of complex food choices. While this process is well‐understood for self‐sufficient organisms, dependent offspring, such as bee larvae, in practice have limited food choices because food is provided by parents. Nutrient balancing may therefore be achieved by offspring, by parents on offspring's behalf, or by both, whether cooperatively or in conflict. We used the Geometric Framework to investigate the capacity of dependent larval mason bees Osmia bicornis to regulate their intake of protein and carbohydrate, as well as these nutrients' effects upon growth and survival. Female Osmia seal eggs individually inside cells they have provisioned with pollen, and have no contact with developing offspring, allowing offspring choices to be studied in isolation. Herbivorous insect larvae are typically expected to balance protein and carbohydrate to maximize growth and reproduction. Contrary to prediction, carbohydrate and not protein mediated both growth and survival to pupation. Accordingly, larvae prioritized maintaining a constant intake of carbohydrate and self‐selected a relatively carbohydrate‐biased diet compared to other hymenopterans, while tolerating wide excesses and deficiencies of protein, rendering them potentially vulnerable to dietary change or manipulation. Reasons for prioritizing carbohydrate may include (a) the relative abundance of protein in their normal pollen diet, (b) the relative paucity of nectar in parental provisions making carbohydrate a scarce resource or (c) the requirement for diapause for all O. bicornis larvae. Larvae were intolerant of moderate dietary dilution, likely reflecting an evolutionary history of nutrient‐dense food. Our results demonstrate that dependent offspring can remain active participants in balancing their own nutrients even when sedentary, and, moreover, even in mass provisioning systems where parents and offspring have no physical contact. Research should now focus on whether and how evolutionary interests of parent and dependent offspring coincide or conflict with respect to food composition, and the implications for species' resilience to changing environments. A free Plain Language Summary can be found within the Supporting Information of this article.

Larval nutrition impacts survival to adulthood, body size and the allometric scaling of metabolic rate in adult honeybees

“…Bees meet all their nutritional demands via pollen and nectar collected from flowers (their main source of protein and carbohydrate, respectively), and unlike the nymphs and larvae of traditional models of insect nutrient regulation, such as locusts and caterpillars, bee larvae are entirely dependent on the provisioning choices of adult bees. This means bee larvae probably have very little opportunity to selectively regulate their intake of nutrients (but see Austin and Gilbert, 2021). Honeybees are unique among bees in that in-hive nurse bees process the pollen and nectar brought back to the nest by foragers, and convert it to a nutritional substance known as royal jelly, which they then regurgitate for larvae (Wright et al, 2018).…”

Variation in nectar quality across 34 grassland plant species

“…The carbohydrate-biased ratios meet the nutritional needs of most flower visitors, e.g. adult honeybee and bumblebee workers, which typically prioritize carbohydrate over (essential) amino acid intake, even over-consuming amino acids to obtain sufficient carbohydrates, and perform generally better on carbohydrate-rich diets (Paoli et al 2014;Stabler et al 2015;Austin & Gilbert 2021). However, (in particular female) butterflies prefer nectars rich in amino acids, and thus likely having lower C:AA ratios, because amino acids increase their fecundity (Mevi-Sch€ utz & Erhardt 2005).…”

Critical links between biodiversity and health in wild bee conservation

“…OPEN ACCESS bicornis) regulate their protein, lipid, and/or carbohydrate intake depending on their age and the presence of brood [91,92]. For these important nutrients, species likely show little tolerance to deviations from the concentrations that best support their performance/fitness, whereas they are likely more tolerant to deviations from concentrations that are less crucial for performance/fitness (as shown for Bombus terrestris [93]).…”

“…As a consequence of the complex and diverse chemistry encountered in different plant species, animals must perform nutrient-selective foraging so as to ensure healthy offspring development [95]. In the case of bees, this means that they should choose pollen with a nutritional composition that matches their nutritional needs, as shown for several bumble bee species that thrive on pollen with high protein to lipid (P:L) ratios and low lipid content [21,96], or O. bicornis bee larvae that prefer diets with a high carbohydrate content [91]. The chemical profile of pollen jointly collected by individual (female) bees of a population can therefore represent a proxy for their species-specific nutritional niche.…”