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.

Keywords: cost-benefit analysis; pitfall trap; plant movement; prey capture; snap trap; suction trap.

Figure 1.

Self-actuated snap traps in the Venus flytrap (D. muscipula) (a) and waterwheel plant (A. vesiculosa) (b). Both species power all steps of the capture process intrinsically. In A. vesiculosa, latch removal is powered synchronously (hydraulic process), but motion actuation during snapping and narrowing combines synchronously and asynchronously powered processes (hydraulics, elastic energy release). In D. muscipula, trap narrowing is actuated solely by synchronously powered hydraulic processes; in Aldrovanda, the elastic energy release is also at play. Both species reopen their traps slowly by synchronously powered hydraulics. Sub-figure (a) modified from [36], in (b) from [49]. (Online version in colour.)

Figure 2.

The suction traps of bladderworts (Utricularia spp.). (a) Top view of the set trap. Note the difference in trap volume owing to the deformation of the elastic sidewalls compared with (e) immediately after suction. (b) Prey bends the trigger hairs on the outer surface of the trapdoor, causing the dome-shaped trap door to snap-buckle and open. The different door configurations are indicated: (i) pre-trigger trapdoor; (ii) inverted curvature after triggering; and (iii) fully opened door. Triggering is powered extrinsically and synchronously by the prey, but latch removal is powered intrinsically and asynchronously by releasing the door's pre-stress during snap-buckling. The process is further accelerated by the inflowing water, driven by the sub-ambient pressure inside the trap. (c) Prey (in this case a daphnid, white outline traced at 0.1 ms intervals) is sucked into the trap. Trap door re-closure (d) is self-actuated by its intrinsic elastic reset force. (e) Immediately after suction, the trap is fully inflated and unable to catch further prey. It is reset though intrinsically powered glands in the trap walls that remove water from the trap interior and pre-stress the trap walls in the process; this resetting takes at least 15 min. After that, the trap is able to catch further prey. (a) and (e) are modified from [47], (b), (c) and (d) from [64]. (Online version in colour.)

Figure 3.

The extrinsically actuated motile springboard-pitfall trap of N. gracilis does not require trigger structures, motors and latches to function. The movement processes are powered extrinsically (i.e. by the impact of raindrops) and synchronously. An ant foraging on the underside of the pitcher lid (highlighted by a dashed white line) is dislodged by the rapid downward acceleration of the lid and falls into the fluid-filled trap. Figure modified from [36].