Kinematical, Structural and Mechanical Adaptations to Desiccation in Poikilohydric Ramonda myconi (Gesneriaceae)

Resurrection plants have fascinated scientists since centuries as they can fully recover from cellular water contents below 10%, concomitantly showing remarkable leaf folding motions. While physiological adaptations have been meticulously investigated, the understanding of structural and mechanical adaptations of this phenomenon is scarce. Using imaging and bending techniques during dehydration-rehydration experiments, morphological, anatomical, and biomechanical properties of desiccation-tolerant Ramonda myconi are examined, and selected structural adaptations are compared to those of homoiohydrous Monophyllaea horsfieldii (both Gesneriaceae). At low water availability, intact and cut-off R. myconi leaves undergo considerable morphological alterations, which are fully and repeatedly reversible upon rehydration. Furthermore, their petioles show a triphasic mechanical behavior having a turgor-based structural stability at high (Phase 1), a flexible mechanically state at intermediate (Phase 2) and a material-based stability at low water contents (Phase 3). Lastly, manipulation experiments with cut-off plant parts revealed that both the shape alterations of individual structures, as well as, the general leaf kinematics largely rely on passive swelling and shrinking processes. Taken together, R. myconi possesses structural and mechanical adaptations to desiccation (in addition to physiological adaptations), which may mainly be passively driven by its water status influenced by the water fluctuations in its surroundings

Different mechanics of snap-trapping in the two closely related carnivorous plants Dionaea muscipula and Aldrovanda vesiculosa

The carnivorous aquatic Waterwheel Plant (Aldrovanda vesiculosa L.) and the closely related terrestrial Venus Flytrap (Dionaea muscipula SOL. EX J. ELLIS) both feature elaborate snap-traps, which shut after reception of an external mechanical stimulus by prey animals. Traditionally, Aldrovanda is considered as a miniature, aquatic Dionaea, an assumption which was already established by Charles Darwin. However, videos of snapping traps from both species suggest completely different closure mechanisms. Indeed, the well-described snapping mechanism in Dionaea comprises abrupt curvature inversion of the two trap lobes, while the closing movement in Aldrovanda involves deformation of the trap midrib but not of the lobes, which do not change curvature. In this paper, we present the first detailed mechanical models for these plants, which are based on the theory of thin solid membranes and explain this difference by showing that the fast snapping of Aldrovanda is due to kinematic amplification of the bending deformation of the midrib, while that of Dionaea unambiguously relies on the buckling instability that affects the two lobes.Comment: accepted in Physical Review

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

The evolutionary roots of carnivory in the Venus flytrap (Dionaea muscipula) stem from a defense response to plant injury caused by, e.g., herbivores. Dionaea muscipula aka. Darwin’s most wonderful plant underwent extensive modification of leaves into snap-traps specialized for prey capture. Even the tiny seedlings of the Venus flytrap already produce fully functional, millimeter-sized traps. The trap size increases as the plant matures, enabling capture of larger prey. The movement of snap-traps is very fast (~100–300 ms) and is actuated by a combination of changes in the hydrostatic pressure of the leaf tissue with the release of prestress (embedded energy), triggering a snap-through of the trap lobes. This instability phenomenon is facilitated by the double curvature of the trap lobes. In contrast, trap reopening is a slower process dependent on trap size and morphology, heavily reliant on turgor and/or cell growth. Once a prey item is caught, the trap reconfigures its shape, seals itself off and forms a digestive cavity allowing the plant to release an enzymatic cocktail to draw nutrition from its captive. Interestingly, a failed attempt to capture prey can come at a heavy cost: the trap can break during reopening, thus losing its functionality. In this mini-review, we provide a detailed account of morphological adaptations and biomechanical processes involved in the trap movement during D. muscipula hunting cycle, and discuss possible reasons for and consequences of trap breakage. We also provide a brief introduction to the biological aspects underlying plant motion and their evolutionary background

Trap diversity and character evolution in carnivorous bladderworts (Utricularia, Lentibulariaceae)

Bladderworts (Utricularia, Lentibulariaceae, Lamiales) constitute the largest genus of carnivorous plants but only aquatic species (about one fifth of the genus) have so far been thoroughly studied as to their suction trap functioning. In this study, we comparatively investigated trap biomechanics in 19 Utricularia species to examine correlations between life-forms, trapping mechanisms, and functional-morphological traits. Our investigations show the existence of two functional trap principles (passive trap in U. multifida vs. active suction traps), and - in active suction traps - three main trapdoor movement types (with several subtypes). The trapdoor movement types and their corresponding functional-morphological features most presumably represent adaptations to the respective habitat. We furthermore give insights into fluid dynamics during suction in three representatives of the main types of trapdoor movement. The results on functional morphology and trapdoor movement were mapped onto a new phylogenetic reconstruction of the genus, derived from the rapidly evolving chloroplast regions trnK, rps16 and trnQ-rps16 and a sampling of 105 Utricularia species in total. We discuss potential scenarios of trap character evolution and species radiation, highlighting possible key innovations that enable such a unique carnivorous lifestyle in different habitats

Chemical Gradients in Polymer-Modified Paper Sheets — Towards Single-Layer Biomimetic Soft Robots

Biomimetic actuators are typically constructed as functional bi- or multilayers, where actuating and resistance layers together dictate bending responses upon triggering by environmental stimuli. Inspired by motile plant structures, like the stems of the false rose of Jericho (Selaginella lepidophylla), we introduce polymer-modified paper sheets that can act as soft robotic single-layer actuators capable of hygro-responsive bending reactions. A tailored gradient modification of the paper sheet along its thickness entails increased dry and wet tensile strength and allows at the same time for hygro-responsiveness. For the fabrication of such single-layer paper devices, the adsorption behavior of a cross-linkable polymer to cellulose fiber networks was first evaluated. By using different concentrations and drying procedures fine-tuned polymer gradients throughout the thickness can be achieved. Due to the covalent cross-linking of polymer with fibers, these paper samples possess significantly increased dry and wet tensile strength properties. We furthermore investigated these gradient papers with respect to a mechanical deflection during humidity cycling. The highest humidity sensitivity is achieved using eucalyptus paper with a grammage of 150 g m⁻² modified with the polymer dissolved in IPA (~13 wt%) possessing a polymer gradient. Our study presents a straightforward approach for the design of novel hygroscopic, paper-based single-layer actuators, which have a high potential for diverse soft robotic and sensor applications

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

Fast snapping in the carnivorous Venus flytrap (Dionaea muscipula) involves trap lobe bending and abrupt curvature inversion (snap‐buckling), but how do these traps reopen? Here, the trap reopening mechanics in two different D. muscipula clones, producing normal‐sized (N traps, max. ≈3 cm in length) and large traps (L traps, max. ≈4.5 cm in length) are investigated. Time‐lapse experiments reveal that both N and L traps can reopen by smooth and continuous outward lobe bending, but only L traps can undergo smooth bending followed by a much faster snap‐through of the lobes. Additionally, L traps can reopen asynchronously, with one of the lobes moving before the other. This study challenges the current consensus on trap reopening, which describes it as a slow, smooth process driven by hydraulics and cell growth and/or expansion. Based on the results gained via three‐dimensional digital image correlation (3D‐DIC), morphological and mechanical investigations, the differences in trap reopening are proposed to stem from a combination of size and slenderness of individual traps. This study elucidates trap reopening processes in the (in)famous Dionaea snap traps – unique shape‐shifting structures of great interest for plant biomechanics, functional morphology, and applications in biomimetics, i.e., soft robotics

Cross-Sectional 4D-Printing: Upscaling Self-Shaping Structures with Differentiated Material Properties Inspired by the Large-Flowered Butterwort (Pinguicula grandiflora)

Extrusion-based 4D-printing, which is an emerging field within additive manufacturing, has enabled the technical transfer of bioinspired self-shaping mechanisms by emulating the functional morphology of motile plant structures (e.g., leaves, petals, capsules). However, restricted by the layer-by-layer extrusion process, much of the resulting works are simplified abstractions of the pinecone scale’s bilayer structure. This paper presents a new method of 4D-printing by rotating the printed axis of the bilayers, which enables the design and fabrication of self-shaping monomaterial systems in cross sections. This research introduces a computational workflow for programming, simulating, and 4D-printing differentiated cross sections with multilayered mechanical properties. Taking inspiration from the large-flowered butterwort (Pinguicula grandiflora), which shows the formation of depressions on its trap leaves upon contact with prey, we investigate the depression formation of bioinspired 4D-printed test structures by varying each depth layer. Cross-sectional 4D-printing expands the design space of bioinspired bilayer mechanisms beyond the XY plane, allows more control in tuning their self-shaping properties, and paves the way toward large-scale 4D-printed structures with high-resolution programmability

Facing the Green Threat: A Water Flea’s Defenses against a Carnivorous Plant

Every ecosystem shows multiple levels of species interactions, which are often difficult to isolate and to classify regarding their specific nature. For most of the observed interactions, it comes down to either competition or consumption. The modes of consumption are various and defined by the nature of the consumed organism, e.g., carnivory, herbivory, as well as the extent of the consumption, e.g., grazing, parasitism. While the majority of consumers are animals, carnivorous plants can also pose a threat to arthropods. Water fleas of the family Daphniidae are keystone species in many lentic ecosystems. As most abundant filter feeders, they link the primary production to higher trophic levels. As a response to the high predatory pressures, water fleas have evolved various inducible defenses against animal predators. Here we show the first example, to our knowledge, in Ceriodaphnia dubia of such inducible defenses of an animal against a coexisting plant predator, i.e., the carnivorous bladderwort (Utricularia x neglecta Lehm, Lentibulariaceae). When the bladderwort is present, C. dubia shows changes in morphology, life history and behavior. While the morphological and behavioral adaptations improve C. dubia’s survival rate in the presence of this predator, the life-history parameters likely reflect trade-offs for the defense

The Structural and Mechanical Basis for Passive‐Hydraulic Pine Cone Actuation

The opening and closing of pine cones is based on the hygroscopic behavior of the individual seed scales around the cone axis, which bend passively in response to changes in environmental humidity. Although prior studies suggest a bilayer architecture consisting of lower actuating (swellable) sclereid and upper restrictive (non‐ or lesser swellable) sclerenchymatous fiber tissue layers to be the structural basis of this behavior, the exact mechanism of how humidity changes are translated into global movement are still unclear. Here, the mechanical and hydraulic properties of each structural component of the scale are investigated to get a holistic picture of their functional interplay. Measurements of the wetting behavior, water uptake, and mechanical measurements are used to analyze the influence of hydration on the different tissues of the cone scales. Furthermore, their dimensional changes during actuation are measured by comparative micro‐computed tomography (µ‐CT) investigations of dry and wet scales, which are corroborated and extended by 3D‐digital image correlation‐based displacement and strain analyses, biomechanical testing of actuation force, and finite element simulations. Altogether, a model allowing a detailed mechanistic understanding of pine cone actuation is developed, which is a prime concept generator for the development of biomimetic hygromorphic systems