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.

Fig. 3.

Friction forces of O. smaragdina ants on the peristome of N. bicalcarata pitchers. (A) O. smaragdina tarsus on the peristome of N. bicalcarata; SEM of live ant. (B) Experimental setup. (C) Example of detachment force recording. (D–F) Friction forces measured on dry vs. wet peristomes and for inward vs. outward pulls. (D) Ants with intact hind legs. (E) Ants with arolia removed (but intact claws). (F) Ants with clipped claws (but intact arolia). Horizontal lines denote medians, boxes mark the inner two quartiles, and whiskers mark the maxima and minima.

Fig. 1.

Nepenthes pitcher and peristome morphology. (A–G) N. bicalcarata. (A) Pitcher. (B) Butterfly (probably Tanaecia pelea pelea) harvesting nectar from the peristome surface. Note the visible line of peristome channels filled with nectar secreted from pores at the inner margin of the peristome (arrow). (C) Underside of inner margin of peristome with tooth-like projections and nectar pores (arrow). (D and E) Peristome surface with first- and second-order radial ridges. Arrows indicate direction toward the inside of the pitcher (F) Transverse section of peristome. Note the transition from the digestive zone to the smooth surface under the peristome (arrow). (G) Inner pitcher wall with digestive gland at the height of the inner peristome margin (H and I) N. alata.(H) Transverse section of peristome. (I) Waxy inner pitcher wall at the height of the inner peristome margin.

Fig. 2.

Initial capture and prey retention in N. bicalcarata. (A) Effect of peristome wetting, drying, and rewetting on the capture efficiency in N. bicalcarata pitchers; O. smaragdina ants. (B) Retention of prey ants in N. bicalcarata pitchers. Data show the condition of ants 30 min after being dropped into the pitcher. Ci, C. inflata; Cc, Camponotus (Colobopsis) sp.; Cs, Camponotus sp.; Ph, P. hector; Pb, Polyrhachis cf. beccarii.