Nutrient Utilization during Male Maturation and Protein Digestion in the Oriental Hornet

Abstract

Males of social Hymenoptera spend the first days following eclosion inside the nest before dispersing to find a young queen to mate with. During this period, they must acquire enough nutrients to enable their sexual maturation and store energy to sustain them through their nuptial journey. It was previously argued that adult hornets are unable to process dietary proteins and rely on the larvae to supply them with free amino acids and carbohydrates that they secrete via trophallaxis. Using isotopically enriched diets, we examined nutrient allocation and protein turnover in newly-emerged males of the Oriental hornet during their maturation period and tested the protein digestion capability in the presence and absence of larvae in both males and worker hornets. The results indicated that protein turnover in males occurs during the first days following eclosion, while carbohydrates are incorporated into body tissues at higher rates towards the end of the maturation period. Additionally, we found that males cannot digest protein and depend on larval secretions as a source of nutrition, while workers, in contrast to previous reports, can metabolize protein independently. Our findings demonstrate the contribution of adult male nutrition and larval secretions to colony fitness.

Continuous exchange of nectar nutrients in an Oriental hornet colony

“…The experiments were conducted in a climate-controlled room (25 ± 2 °C, 75 ± 10% RH). We used bumble bees (Bombus terrestris), a common protein source for hornets 10,54 , to feed the experimental colonies, according to our experimental design. The bumble bee colony was purchased from AgroBee, Ein Yahav, Israel.…”

“…In contrast, for the larvae, this exchange is generally unidirectional, as larvae are sessile and must receive their food from adults 6 . In some species of hymenopterans, however, the larvae secrete a liquid back to the adults that facilitates food-processing by the adults 9,10 . In the fire ant Solenopsis invicta and the leaf-cutter ant Acromyrmex subterraneus, the larvae possess a higher and more diverse digestive enzymatic profile than that of the adults 11,12 .…”

“…Wasp larvae are fed with prey (arthropod or carrion) collected by adults and, in exchange, the larvae deliver back to the adults the protein degradation products as a secretion containing simple carbohydrates and free amino acids (resulting from gluconeogenesis and protein breakdown, respectively) 14,17 . Although wasp workers can partially digest the proteins obtained from their prey, males are unable to do so and rely entirely on larvae for protein digestion 10 . This both reciprocal and unilateral exchange of nutrients (i.e., protein versus carbohydrates and free amino acids), and consequent nutritional co-dependency between adults and larvae, is suggested to be key to establishing sociality in Vespidae 10,15 .…”

“…Although wasp workers can partially digest the proteins obtained from their prey, males are unable to do so and rely entirely on larvae for protein digestion 10 . This both reciprocal and unilateral exchange of nutrients (i.e., protein versus carbohydrates and free amino acids), and consequent nutritional co-dependency between adults and larvae, is suggested to be key to establishing sociality in Vespidae 10,15 .…”

“…While these methods have provided valuable information on the food exchange dynamics within the colony, they are limited by the constraints of labeling the food resources as a whole. In contrast, using stable isotopically-labeled macronutrients enables the study of how a specific nutrient, or even a specific carbon, present in the food resource is transferred, allocated, and utilized by each colony member 10,36 .…”