The geometry of dependence: solitary bee larvae prioritize carbohydrate over protein in parentally provided pollen

Bees, important pollinators, have declined significantly in recent decades, and human- induced changes to nutritional landscapes are partly responsible. Changes to nutritional quality rather than quantity have been overlooked as a threat to bee health. Yet knowledge of bee nutrition is currently largely restricted to adults of social species. Larval stages, where most growth occurs, are relatively understudied - perhaps because most social bees provision progressively and collectively, making nutrition difficult to trace. In mass-provisioning solitary bees ( Osmia bicornis L.), we can manipulate and follow larval nutrition, and thereby determine effects of changes in diet quality. Under the Geometric Framework for Nutrition, we restricted larvae to 6 diets: 3 protein:carbohydrate ratios and 2 nutrient concentrations. We asked: (a) which diets maximise body size and survival, (b) what consumption rules do larvae follow when nutrients are imbalanced? Finally, (c) given a choice of complementary diets, are larvae able to select a dietary balance? Larvae pupated after consuming a fixed carbohydrate amount, but tolerated a wide range of protein. Body size and survival were maximised on our lowest P:C ratio diet, and having consumed the most carbohydrate. When eating freely from two diets, larvae converged on a P:C ratio of 1:1.8, but not an overall nutrient intake target. Nevertheless, larvae maintained stable carbohydrate intake, while protein intake varied with the available diet. Our results suggest solitary bee larvae regulate carbohydrate most closely, but that excessive indigestible material may limit their actual nutrient intake. Carbohydrate may be critical to overwinter survival, and/or may be more limiting than protein. The large variation in protein tolerated, despite its importance, suggests bee larvae may be vulnerable to landscape changes - and therefore reliant on parents to regulate protein. Given the mixed evidence on whether parents can sense pollen protein content, our results highlight bees’ potential vulnerability to a “nutritional trap”, i.e. where rapid changes in their nutritional environment outstrip their evolved capacity to detect those changes, impairing their fitness.