Insect aquaplaning: Nepenthes pitcher plants capture prey with the peristome, a fully wettable water-lubricated anisotropic surface

Abstract

Pitcher plants of the genus Nepenthes have highly specialized leaves adapted to attract, capture, retain, and digest arthropod prey. Several mechanisms have been proposed for the capture of insects, ranging from slippery epicuticular wax crystals to downward-pointing lunate cells and alkaloid secretions that anesthetize insects. Here we report that perhaps the most important capture mechanism has thus far remained overlooked. It is based on special surface properties of the pitcher rim (peristome) and insect ''aquaplaning.'' The peristome is characterized by a regular microstructure with radial ridges of smooth overlapping epidermal cells, which form a series of steps toward the pitcher inside. This surface is completely wettable by nectar secreted at the inner margin of the peristome and by rain water, so that homogenous liquid films cover the surface under humid weather conditions. Only when wet, the peristome surface is slippery for insects, so that most ant visitors become trapped. By measuring friction forces of weaver ants (Oecophylla smaragdina) on the peristome surface of Nepenthes bicalcarata, we demonstrate that the two factors preventing insect attachment to the peristome, i.e., water lubrication and anisotropic surface topography, are effective against different attachment structures of the insect tarsus. Peristome water films disrupt attachment only for the soft adhesive pads but not for the claws, whereas surface topography leads to anisotropic friction only for the claws but not for the adhesive pads. Experiments on Nepenthes alata show that the trapping mechanism of the peristome is also essential in Nepenthes species with waxy inner pitcher walls.

Harmless nectar source or deadly trap:Nepenthespitchers are activated by rain, condensation and nectar

“…These findings confirm the importance of the peristome and of 'insect aquaplaning' for prey capture by Nepenthes species (Bohn & Federle 2004) under field conditions. Although the running experiments with ants did not represent natural capture events, they accurately indicate the effectiveness of the pitcher traps.…”

“…We investigated whether experimental wetting of the peristome in N. rafflesiana var. typica pitchers increased the capture efficiency, as we demonstrated previously for Nepenthes bicalcarata (Bohn & Federle 2004). We tested the effects of wetting (using an atomizer), drying (with dust-free tissue) and re-wetting (see figure S1 and video in the electronic supplementary material).…”

“…When the peristome is wet, the fluid films prevent the insects' tarsal adhesive pads from making close contact with the surface, similar to the aquaplaning of a car tyre on a wet road. In addition, the anisotropic microstructure of the peristome surface allows interlocking of claws only while the insect is running towards the pitcher inside, but not on the way out (Bohn & Federle 2004). …”

‘Insect aquaplaning’ on a superhydrophilic hairy surface: howHeliamphora nutansBenth. pitcher plants capture prey

“…The evolution of specialized superhydrophilic trapping surfaces in two different plant orders provides a striking example of trait convergence. In both taxa, experimental ablation of arolia neutralized the effect of wetness on the friction forces of ant tarsi, confirming that wetting is effective against the insects' adhesive pads [19]. In addition, the microstructure of both surfaces shows a strong inward-outward anisotropy that allows interlocking only in one direction.…”

Locomotion and attachment of leaf beetle larvaeGastrophysa viridula(Coleoptera, Chrysomelidae)

“…Adult G. viridula slid continuously when centrifuged, suggesting either an aquaplaning-like effect [64] or stick-and-slip reduction owing to the presence of multiple minute contacts instead of one or few larger ones [65,66]. Owing to multiple minute contacts, stickand-slip events happen at each single contact, but at different times.…”