Mechanism for rapid passive-dynamic prey capture in a pitcher plant

Abstract

Plants use rapid movements to disperse seed, spores, or pollen and catch animal prey. Most rapid-release mechanisms only work once and, if repeatable, regaining the prerelease state is a slow and costly process. We present an encompassing mechanism for a rapid, repeatable, passive-dynamic motion used by a carnivorous pitcher plant to catch prey. Nepenthes gracilis uses the impact of rain drops to catapult insects from the underside of the canopy-like pitcher lid into the fluid-filled trap below. High-speed video and laser vibrometry revealed that the lid acts as a torsional spring system, driven by rain drops. During the initial downstroke, the tip of the lid reached peak velocities similar to fast animal motions and an order of magnitude faster than the snap traps of Venus flytraps and catapulting tentacles of the sundew Drosera glanduligera. In contrast to these active movements, the N. gracilis lid oscillation requires neither mechanical preloading nor metabolic energy, and its repeatability is only limited by the intensity and duration of rainfall. The underside of the lid is coated with friction-reducing wax crystals, making insects more vulnerable to perturbations. We show that the trapping success of N. gracilis relies on the combination of material stiffness adapted for momentum transfer and the antiadhesive properties of the wax crystal surface. The impact-driven oscillation of the N. gracilis lid represents a new kind of rapid plant movement with adaptive function. Our findings establish the existence of a continuum between active and passive trapping mechanisms in carnivorous plants.

Comparative kinematical analyses of Venus flytrap (Dionaea muscipula) snap traps

“…As a conclusion it can be said that the Venus flytrap has evolved a remarkable trapping system that functions as well in air as under water, and which can be considered as an optimized system for nutrient acquisition of a carnivorous plant growing in seasonally inundated habitats. Similar reports on carnivorous plants with traps functioning under different environmental conditions are, e.g., the resinous Roridula sticky traps [ 37 ] and the rainwater-dependent pitfall trapping systems in Nepenthes [ 38 – 39 ]. The Dionaea trap is not “only” a “simple” snap trap but possesses different snapping modes, movement mechanics and actuation principles, which greatly broadens our understanding of this (in)famous carnivore and opens up novel perspectives for future studies.…”

Convergent and divergent evolution in carnivorous pitcher plant traps

“…For example, Bauer et al . () demonstrated that the pitcher lid of N. gracilis is adapted to exploit the impact of rain drops for capturing insect prey. The lid of this species functions as a rain‐driven torsion spring, flicking insects into the pitcher during heavy rain.…”

“…Modifications in trap geometry may enable the utilization of novel nutrient sources, analogous to well-known examples in animals, such as the diverse beak shapes of Darwin's finches and the various adaptations of cichlid fish in the African Great Lakes. For example, Bauer et al (2015a) demonstrated that the pitcher lid of N. gracilis is adapted to exploit the impact of rain drops for capturing insect prey. The lid of this species functions as a rain-driven torsion spring, flicking insects into the pitcher during heavy rain.…”

Contributions of lunate cells and wax crystals to the surface anisotropy ofNepenthesslippery zone

“…Considering the significant differences in macromorphology, microstructure and their corresponding functions, the pitchers can be typically divided into four parts: a canopy-like lid, a collar-formed peristome, a slippery zone and a digestive zone [ 5 , 6 ]. The canopy-like lid prevents the inner pitcher from being contaminated [ 7 ], also acts as a catapult to make insects fall into the pitcher below [ 8 ]. The collar-formed peristome consists of radial ridges, which extend towards the pitcher inside [ 2 , 9 , 10 ].…”