Tactile active sensing in insect-plant pollination

Abstract

The interaction between insects and the flowers they pollinate has driven the evolutionary diversity of both insects and flowering plants, two groups with the most numerous species on earth. Insects use vision and olfaction to localize their host plants, but to feed from the flower, they must find the tiny nectary opening, which can be well beyond their visual resolution. When vision is limited, the sense of touch becomes especially crucial, yet very few studies have investigated the role of rapid and precise tactile feedback in successful feeding and pollination interactions. In this paper, we study the remarkable feeding behavior of flying insects that use their proboscis, a flexible mouthpart often longer than their entire body length when unfurled, to expertly explore floral surfaces. Specifically, we observed how the crepuscular hawkmoth Manduca sexta interacts with artificial, 3D-printed flowers of varying shapes. We found that moths actively explore the flower for tactile features, systematically sweeping their proboscis from edge to center repeatedly until they locate the nectary. Moreover, naive moths rapidly learn to exploit flowers, and they adopt a tactile search strategy to more directly locate the nectary in as few as three to five consecutive visits. We suggest moths wield their proboscis to extract salient tactile features, such as floral edges and corolla curvature. Our results highlight the proboscis as a unique sensory structure and emphasize the central role of touch in insect-plant pollination interactions.