Slippery surfaces of pitcher plants: Nepenthes wax crystals minimize insect attachment via microscopic surface roughness

Pitcher plants of the genus Nepenthes efficiently trap and retain insect prey in highly specialized leaves. Besides a slippery peristome which inhibits adhesion of insects they employ epicuticular wax crystals on the inner walls of the conductive zone of the pitchers to hamper insect attachment by adhesive devices. It has been proposed that the detachment of individual crystals and the resulting contamination of adhesive organs is responsible for capturing insects. However, our results provide evidence in favour of a different mechanism, mainly based on the stability and the roughness of the waxy surface. First, we were unable to detect a large quantity of crystal fragments on the pads of insects detached from mature pitcher surfaces of Nepenthes alata. Second, investigation of the pitcher surface by focused ion beam treatment showed that the wax crystals form a compact 3D structure. Third, atomic force microscopy of the platelet-shaped crystals revealed that the crystals are mechanically stable, rendering crystal detachment by insect pads unlikely. Fourth, the surface profile parameters of the wax layer showed striking similarities to those of polishing paper with low grain size. By measuring friction forces of insects on this artificial surface we demonstrate that microscopic roughness alone is sufficient to minimize insect attachment. A theoretical model shows that surface roughness within a certain length scale will prevent adhesion by being too rough for adhesive pads but not rough enough for claws.