A specialized bird pollination system with a bellows mechanism for pollen transfer and staminal food body rewards

Bird pollination has evolved repeatedly among flowering plants but is almost exclusively characterized by passive transfer of pollen onto the bird and by nectar as primary reward [1, 2]. Food body rewards are exceedingly rare among eudicot flowering plants and are only known to occur on sterile floral organs [3]. In this study, we report an alternative bird pollination mechanism involving bulbous stamen appendages in the Neotropical genus Axinaea (Melastomataceae). We studied the pollination process by combining pollination experiments, video monitoring, and detailed analyses of stamen structure and metabolomic composition. We show that the bulbous stamen appendages, which are consumed by various species of passerines (Thraupidae, Fringillidae), are bifunctional during the pollination process. First, the appendages work as bellows organs in a unique pollen expulsion mechanism activated by the passerines. As the birds seize an appendage with their beaks in order to remove it from the flower for consumption, air contained in the appendage's aerenchymatous tissue is pressed into the hollow anther. The resulting air flow causes the expulsion of a pollen jet and the deposition of pollen on the bird's head and beak. Second, the stamen appendages provide a hexose-rich, highly nutritious (15,100 J/g) food body reward for the pollinating passerines. This discovery expands our knowledge of flowering plant pollination systems and provides the first report of highly specialized bellows organs for active pollen transfer in flowering plants. In addition, this is the only known case of a food body reward associated with reproductive structures in the eudicot clade of flowering plants.