Ecological function of the 'elephant trunk' upper corolla in Pedicularis species

The evolution of intricate floral structures is often a direct consequence of pollinator-mediated selection. In buzz-pollinated plants, pollen is released through vibrations, and control of its removal is crucial for maximizing male reproductive success. The genus Pedicularis presents a compelling case, with many species exhibiting a distinctive upper corolla lip, or galea, shaped like a 'beak' or 'elephant trunk'. The adaptive function of this trait has remained mysterious and largely not subjected to empirical testing. We hypothesized that the beak acts as a dispensing tunnel or poricidal anther, restricting pollen removal by bumblebee pollinators.

To test this hypothesis, we conducted a comparative field study on three sympatric wild species in the Hengduan Mountains: the beakless Pedicularis densispica, the short-beaked Pedicularis cephalantha and the long-beaked Pedicularis rhinanthoides. All three species share the bumblebee Bombus friseanus as their exclusive pollinator. Our integrative methodology combined detailed observations of pollinator foraging behaviour, direct quantification of pollen removal and deposition per single visit, and controlled laboratory experiments using floral models with pollen analogues to isolate the mechanical effects of beak architecture.

We found that beakless P. densispica experienced higher visitation frequency but shorter per-flower visit duration. Bumblebees spent a longer time on the two beaked Pedicularis; however, short-beaked species had nearly twice the proportional pollen removal compared with long-beaked species. Furthermore, artificial buzzes on floral models confirmed that longer, curved beaks reduced pollen analogue removal.

Collectively, our findings indicate that the beak structure functions as a pollen-dispensing mechanism, controlling pollen removal in Pedicularis. This first empirical study on the ecological function of the Pedicularis 'elephant trunk' offers crucial insights into floral trait evolution within this diversifying genus, highlighting how specific complicated floral morphologies can tune pollen removal in buzz-pollinated plants.