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

Simple Summary The Oriental hornet is a notorious bee predator that is well adapted to arid habitats. Under favorable conditions, due to ongoing climate change, it is actively spreading northward in Europe and Central Asia and was recently introduced to the Americas. As a eusocial insect, it forms annual colonies consisting of a foundress queen, sterile workers, brood, and, towards the end of the colony's life-cycle, also male reproductives. In the present study, we examined nutritional processes in the Oriental hornet, focusing on the neglected caste of male reproductives, to assess the involvement of nutrition in the colony's reproductive success. We used stable isotope labelled nutrients to investigate the metabolic processes occurring in adult males as they mature inside the nest, assessing the protein digestion capacity in the male and worker castes and evaluating the contribution of larvae to this process. The results showed that, in the body of maturing males, dietary amino acids are utilized first in the synthesis of proteins, then carbohydrates are allocated into tissues as energy reserves. We discovered that adult workers can process dietary proteins independently (contrary to previous knowledge), while males cannot and rely entirely on the larvae to process proteins for them. Larval secretions were found to contribute significantly to protein uptake by both males and workers. We suggest that larval secretions are a central nutritional resource for adult hornets that play a key role in maintaining the social structure in the colony. 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.