Complexity and diversity of motion amplification and control strategies in motile carnivorous plant traps

Abstract

Similar to animals, plants have evolved mechanisms for elastic energy storage and release to power and control rapid motion, yet both groups have been largely studied in isolation. This is exacerbated by the lack of consistent terminology and conceptual frameworks describing elastically powered motion in both groups. Iconic examples of fast movements can be found in carnivorous plants, which have become important models to study biomechanics, developmental processes, evolution and ecology. Trapping structures and processes vary considerably between different carnivorous plant groups. Using snap traps, suction traps and springboard-pitfall traps as examples, we illustrate how traps mix and match various mechanisms to power, trigger and actuate motions that contribute to prey capture, retention and digestion. We highlight a fundamental trade-off between energetic investment and movement control and discuss it in a functional-ecological context.

Shapeshifting in the Venus flytrap (Dionaea muscipula): Morphological and biomechanical adaptations and the potential costs of a failed hunting cycle

“…Once triggered, the doubly curved D. muscipula snap-traps undergo hydraulically driven lobe deformation (Hedrich and Neher, 2018;Scherzer et al, 2019;Bauer et al, 2021) generating a buckling instability (Forterre et al, 2005;Poppinga and Joyeux, 2011;Sachse et al, 2020). Thus accumulated elastic energy is then released during snap-through of the trap, where the geometry of the trap lobes changes from concave to convex (Figures 1B,C) due to snap-buckling-a motion performed between 100 and 300 ms (Forterre, 2013).…”

“…The subsequent trap actuation and deformation processes involved in prey retention and digeston in traps of the juvenile plants are completely unknown so far (indicated by question marks). Images of traps from the juvenile plants were adapted fromPoppinga et al (2016), images of traps of the adult plants were adapted fromBauer et al (2021).…”

Smooth or with a Snap! Biomechanics of Trap Reopening in the Venus Flytrap (Dionaea muscipula)

“…[ 1 , 2 , 3 ] It gained notoriety due to its spectacular ability to capture prey via snap trap closure, which can be executed in as little as 100 ms. [ 3 ] The fast snapping motion relies on a “smart” combination of hydraulic cellular processes with rapid release of stored elastic energy arising from prestress due to internal growth processes and hydrostatic pressure, which trigger the snap‐through. [ 3 , 4 , 5 ] The snap‐through motion itself is a mechanical instability phenomenon affecting the doubly curved lobes of the traps. [ 4 ] In contrast, trap reopening is a much slower process, of which duration depends on whether the trap remained empty following closure or if a food item was successfully trapped following mechanical stimulation by the prey (mainly arthropods).…”

Pitcher geometry facilitates extrinsically powered ‘springboard trapping' in carnivorousNepenthes gracilispitcher plants

“…Instead, they employ growth or water transport processes to accumulate elastic energy, which is suddenly released via snap-buckling or explosive fracture [ 2 ]. Whist these spring mechanisms generate astonishingly fast movements [ 3 ], they require time and metabolic energy for preloading [ 4 ]. For a carnivorous plant, this could mean missing a catch because the trap is not ready.…”

“…For a carnivorous plant, this could mean missing a catch because the trap is not ready. The pitcher plant Nepenthes gracilis solved this problem elegantly: it exploits falling rain drops to generate a fast and instantaneous trap movement free of metabolic costs [ 4 , 5 ].…”