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

Abstract

Although the Venus flytrap (Dionaea muscipula) can be considered as one of the most extensively investigated carnivorous plants, knowledge is still scarce about diversity of the snap-trap motion, the functionality of snap traps under varying environmental conditions, and their opening motion. By conducting simple snap-trap closure experiments in air and under water, we present striking evidence that adult Dionaea snaps similarly fast in aerial and submersed states and, hence, is potentially able to gain nutrients from fast aquatic prey during seasonal inundation. We reveal three snapping modes of adult traps, all incorporating snap buckling, and show that millimeter-sized, much slower seedling traps do not yet incorporate such elastic instabilities. Moreover, opening kinematics of young and adult Dionaea snap traps reveal that reverse snap buckling is not performed, corroborating the assumption that growth takes place on certain trap lobe regions. Our findings are discussed in an evolutionary, biomechanical, functional-morphological and biomimetic context.

Keywords: Droseraceae; biomechanics; carnivorous plant; fast plant movement; functional morphology.

Figure 1

A closed Dionaea muscipula trap. Petiole and leaf blade serve the function of photosynthesis. In addition, the leaf blade is highly modified and contains a midrib which connects the two trap lobes. On the upper margins of the lobes, several “teeth” are located which interlock in the closed state of the trap. Trap lengths as presented in this article were measured as indicated.

Figure 2

Statistical analyses of the comparative air/water snapping experiment. (a) Boxplot comparison of trap lengths in air and under water. The sample sizes for each surrounding medium is n = 30. The trap lengths are not significantly different between the different surrounding media (Wilcoxon rank sum test, W = 487.5; p > 0.05). (b) Boxplot comparison of snapping durations in air and under water. The sample sizes for each surrounding medium is n = 30. The snapping durations are not significantly different between the different surrounding media (Wilcoxon rank sum test, W = 472; p > 0.05). (c) Snapping durations do not correlate significantly with the trap lengths (Spearman‘s rho = −0.21). The regression line is indicated.

Figure 3

Snapping modes of Venus flytrap. (a) Synchronous lobe movements either lead to a sudden curvature inversion of both trap lobes (“normal” snapping), or (b) to a snap buckling beginning at the apical part of the trap and progressing towards the basal part. (c) In asynchronous trap lobes, one of the lobes moves first. Time scales are indicated, arrows depict lobe movement. At t = 0.29 s in (a), the trap is in the state defined as the closed state in this article (see Experimental section). Afterwards, the poroelastically dampened closure motion proceeds, but much slower (see timescales).

Figure 4

Snapping of a trap under water. Time scale is indicated. An ink filament reaching into the trap with the ink drop is visible. During snapping, no noticeable distortion of the filament, but an outflow of bulk ink out of small gaps at the lateral trap parts is visible. The trap lobes move asynchronously, whereby the triggered lobe (the left lobe in the images) moves first. Images are from Supporting Information File 8.

Figure 5

Seedling and adult traps. (a) A seedling trap in the open and closed state, the opening angle is indicated. (b) An adult trap in the open and closed state, the opening angle is indicated. (c) Seedlings cultivated in the Botanic Garden Freiburg often showed arthropod remnants inside the traps, indicating successful prey capture. (d) Section of a seedling trap. (e) Section of an adult trap. (d) and (e) were used for approximations of lobe thicknesses required for calculations in the discussion.

Figure 6

Statistical analyses of the comparative seedling trap/adult trap snapping experiment. (a) Boxplot comparison of trap lengths in different developmental stages of the Venus flytrap. The sample size for adult traps is n = 21 (see Experimental section), for seedlings n = 12. The trap lengths are highly significantly different between the two growth stages. (b) Boxplot comparison of snapping durations in different developmental stages of the Venus flytrap. The sample size for adult traps is n = 21 (see Experimental section), for seedlings n = 12. The snapping durations for adult traps are highly significantly shorter than for seedling traps. (c) Snapping durations do not correlate with the trap lengths in seedlings (Spearman‘s rho = −0.21).

Figure 7

Comparative kinematics of closing and opening motions in adult and seedling traps. Note the different time scales indicated. The adult trap closes very rapidly and performs a sudden geometrical change (snap buckling, indicated by dashed grey lines), whereas the much slower closing of the seedling trap is a very continuous process without any noticeable acceleration. Opening traps also move very continuously, indicating that no reverse snap-buckling takes place either in the adult traps or in the seedling traps. The normalized distance d* is calculated as ratio of d, the remaining distance between the lobes measured for various phases of closure, over d_max, the distance between the lobes in the fully open trap.