Snapping mechanics of the Venus flytrap (Dionaea muscipula)

Abstract

The mechanical principles for fast snapping in the iconic Venus flytrap are not yet fully understood. In this study, we obtained time-resolved strain distributions via three-dimensional digital image correlation (DIC) for the outer and inner trap-lobe surfaces throughout the closing motion. In combination with finite element models, the various possible contributions of the trap tissue layers were investigated with respect to the trap's movement behavior and the amount of strain required for snapping. Supported by in vivo experiments, we show that full trap turgescence is a mechanical-physiological prerequisite for successful (fast and geometrically correct) snapping, driven by differential tissue changes (swelling, shrinking, or no contribution). These are probably the result of the previous accumulation of internal hydrostatic pressure (prestress), which is released after trap triggering. Our research leads to an in-depth mechanical understanding of a complex plant movement incorporating various actuation principles.

Keywords: elastic instability; finite element modeling; plant biomechanics; plant movement; snap-buckling.

Fig. 1.

Computed trap models with various strain distributions and layer setups without prestress. (A) Measured strain distributions and various load cases for simulations with transformation of coordinate systems. Relationships between opening angle and maximum absolute strain (B) for measured strain distributions and (C) for interpolated strain distributions in all layer setups. The abbreviations correspond to the number of tissue layers (three or two), the behavior of these layers during closure (expansion, +; contraction, −; no actuation, 0), and the extent of expansion or contraction (in %). Moreover, the relative thicknesses of the tissue layers are depicted (see SI Appendix for more details). The only models performing snap-through are the bilayered 2+−100 (inner epidermis contracts as much as the outer epidermis expands) measured load case (B1) and interpolated load case (C1), which, however, do not fit the observed geometrical behavior of the real trap (Movies S7 and S8). Details for all models can be extracted from SI Appendix, Fig. S2.

Fig. 2.

Computed trap models with various strain distributions and layer setups including prestress. Relationship between opening angle and maximum applied strain (A) for measured strain distribution and (B) for interpolated strain distribution for all layer setups including a prestress process as predicted by model 2. The abbreviations correspond to the number of tissue layers (three or two), the behavior of these layers during closure (expansion, +; contraction, −; no actuation, 0), and the extent of expansion or contraction (in %) (see SI Appendix for more details). (C1) Dehydrated trap with larger opening angle. (C2) Trap in ready-to-snap configuration with smaller opening angle. (C3) Closed trap. Deformation states of model 2 for models most closely resembling the snap-trapping: (D1) With layer setup 3+00 (outer epidermis expands, and middle and inner layers remain neutral) in zero-stress state. (D2) After loading with the prestress strain, in ready-to-snap configuration, and (D3) after loading with the closing strain (representing the quantitative strain value measured in the DIC experiments; Fig. 1), in closed configuration. Deformation states for layer setup (E1–E3) 3+0−20 (outer epidermis expands, middle layer remains neutral, and inner epidermis contracts by 20% relative to outer epidermal expansion) and (F1–F3) 3+0−100 (outer epidermis expands, middle layer remains neutral, and inner epidermis contracts as much as outer epidermis). Details for all models can be extracted from SI Appendix, Fig. S3.

Fig. 3.

Effect of various hydration states (fully hydrated, dehydrated, rehydrated) on D. muscipula traps (n = 9) with regard to opening angle (Left), RWC (Middle), and snapping duration (Right). For trapping duration, only three traps (red dots) responded to triggering in the dehydrated state.

Fig. 4.

FE model basics. FE model (A) of original geometry and (B) of further opened geometry of D. muscipula with dimensions according to the biological specimen. (C) Cross-section of a typical D. muscipula trap showing a linear tapering from base to top. (D) Overview of used units and model parameters according to literature.