Snapping mechanics of the Venus flytrap (Dionaea muscipula).

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.

Are cyclic plant and animal behaviours driven by gravimetric mechanical forces?

The celestial mechanics of the Sun, Moon, and Earth dominate the variations in gravitational force that all matter, live or inert, experiences on Earth. Expressed as gravimetric tides, these variations are pervasive and have forever been part of the physical ecology with which organisms evolved. Here, we first offer a brief review of previously proposed explanations that gravimetric tides constitute a tangible and potent force shaping the rhythmic activities of organisms. Through meta-analysis, we then interrogate data from three study cases and show the close association between the omnipresent gravimetric tides and cyclic activity. As exemplified by free-running cyclic locomotor activity in isopods, reproductive effort in coral, and modulation of growth in seedlings, biological rhythms coincide with temporal patterns of the local gravimetric tide. These data reveal that, in the presumed absence of rhythmic cues such as light and temperature, local gravimetric tide is sufficient to entrain cyclic behaviour. The present evidence thus questions the phenomenological significance of so-called free-run experiments.

Rapid flower closure of Drosera tokaiensis deters caterpillar herbivory.

Certain plants exhibit rapid movement in response to mechanical stimulation; however, the ecological functions of this behaviour are largely unknown. Here, we show that the rapid flower closure of Drosera tokaiensis (Droseraceae) in response to mechanical stimulation functions as a physical defence against a specialist herbivore Buckleria paludum (Pterophoridae) caterpillar. Following feeding damage on fruits, flowers, flower stalks and buds by B. paludum, D. tokaiensis closed its flowers nine times faster than during natural circadian closure. The extent of damage to ovules was significantly reduced when the flowers were able to close compared with the condition in which closure was physically inhibited by the application of a resin. Nonetheless, flower closure had no effect on the feeding damage to stamens and styles and promoted further damage to petals. Given that feeding on petals, stamens and styles had no significant effect on the number of mature seeds, rapid flower closure leading to the protection of ovules had an overall positive effect on the reproductive success of D. tokaiensis. Our study showed rapid plant movement as a novel case of induced physical defence against herbivory.

Pitcher geometry facilitates extrinsically powered 'springboard trapping' in carnivorous Nepenthes gracilis pitcher plants.

Carnivorous pitcher plants capture insects in cup-shaped leaves that function as motionless pitfall traps. Nepenthes gracilis evolved a unique 'springboard' trapping mechanism that exploits the impact energy of falling raindrops to actuate a fast pivoting motion of the canopy-like pitcher lid. We superimposed multiple computed micro-tomography images of the same pitcher to reveal distinct deformation patterns in lid-trapping N. gracilis and closely related pitfall-trapping N. rafflesiana. We found prominent differences between downward and upward lid displacement in N. gracilis only. Downward displacement was characterized by bending in two distinct deformation zones whist upward displacement was accomplished by evenly distributed straightening of the entire upper rear section of the pitcher. This suggests an anisotropic impact response, which may help to maximize initial jerk forces for prey capture, as well as the subsequent damping of the oscillation. Our results point to a key role of pitcher geometry for effective 'springboard' trapping in N. gracilis.

ZEITLUPE facilitates the rhythmic movements of Nicotiana attenuata flowers.

Circadian organ movements are ubiquitous in plants. These rhythmic outputs are thought to be regulated by the circadian clock and auxin signalling, but the underlying mechanisms have not been clarified. Flowers of Nicotiana attenuata change their orientation during the daytime through a 140° arc to balance the need for pollinators and the protection of their reproductive organs. This rhythmic trait is under the control of the circadian clock and results from bending and re-straightening movements of the pedicel, stems that connect flowers to the inflorescence. Using an explant system that allowed pedicel growth and curvature responses to be characterized with high spatial and temporal resolution, we demonstrated that this movement is organ autonomous and mediated by auxin. Changes in the growth curvature of the pedicel are accompanied by an auxin gradient and dorsiventral asymmetry in auxin-dependent transcriptional responses; application of auxin transport inhibitors influenced the normal movements of this organ. Silencing the expression of the circadian clock component ZEITLUPE (ZTL) arrested changes in the growth curvature of the pedicel and altered auxin signalling and responses. IAA19-like, an Aux/IAA transcriptional repressor that is circadian regulated and differentially expressed between opposite tissues of the pedicel, and therefore possibly involved in the regulation of changes in organ curvature, physically interacted with ZTL. Together, these results are consistent with a direct link between the circadian clock and the auxin signalling pathway in the regulation of this rhythmic floral movement.

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

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.

A water drop-shaped slingshot in plants: geometry and mechanics in the explosive seed dispersal of Orixa japonica (Rutaceae).

BACKGROUND AND AIMS: In angiosperms, many species disperse their seeds autonomously by rapid movement of the pericarp. The fruits of these species often have long rod- or long plate-shaped pericarps, which are suitable for ejecting seeds during fruit dehiscence by bending or coiling. However, here we show that fruit with a completely different shape can also rely on pericarp movement to disperse seeds explosively, as in Orixa japonica. METHODS: Fruit morphology was observed by hard tissue sectioning, scanning electron microscopy and micro-computed tomography, and the seed dispersal process was analysed using a high-speed camera. Comparisons were made of the geometric characteristics of pericarps before and after fruit dehiscence, and the mechanical process of pericarp movement was simulated with the aid of the finite element model. KEY RESULTS: During fruit dehydration, the water drop-shaped endocarp of O. japonica with sandwich structure produced two-way bending deformation and cracking, and its width increased more than three-fold before opening. Meanwhile the same shaped exocarp with uniform structure could only produce small passive deformation under relatively large external forces. The endocarp forced the exocarp to open by hygroscopic movement before seed launching, and the exocarp provided the acceleration for seed launching through a reaction force. CONCLUSIONS: Two layers of water drop-shaped pericarp in O. japonica form a structure similar to a slingshot, which launches the seed at high speed during fruit dehiscence. The results suggest that plants with explosive seed dispersal appear to have a wide variety of fruit morphology, and through a combination of different external shapes and internal structures, they are able to move rapidly using many sophisticated mechanisms.

The hook shape of growing leaves results from an active regulatory process.

The rachis of most growing compound leaves observed in nature exhibits a stereotypical hook shape. In this study, we focus on the canonical case of Averrhoa carambola. Combining kinematics and mechanical investigation, we characterize this hook shape and shed light on its establishment and maintenance. We show quantitatively that the hook shape is a conserved bent zone propagating at constant velocity and constant distance from the apex throughout development. A simple mechanical test reveals non-zero intrinsic curvature profiles for the rachis during its growth, indicating that the hook shape is actively regulated. We show a robust spatial organization of growth, curvature, rigidity, and lignification, and their interplay. Regulatory processes appear to be specifically localized: in particular, differential growth occurs where the elongation rate drops. Finally, impairing the graviception of the leaf on a clinostat led to reduced hook curvature but not to its loss. Altogether, our results suggest a role for proprioception in the regulation of the leaf hook shape, likely mediated via mechanical strain.

Functional-morphological analyses of the delicate snap-traps of the aquatic carnivorous waterwheel plant (Aldrovanda vesiculosa) with 2D and 3D imaging techniques.

BACKGROUND AND AIMS: The endangered aquatic carnivorous waterwheel plant (Aldrovanda vesiculosa) catches prey with 3-5-mm-long underwater snap-traps. Trapping lasts 10-20 ms, which is 10-fold faster than in its famous sister, the terrestrial Venus flytrap (Dionaea muscipula). After successful capture, the trap narrows further and forms a 'stomach' for the digestion of prey, the so-called 'sickle-shaped cavity'. To date, knowledge is very scarce regarding the deformation process during narrowing and consequent functional morphology of the trap. METHODS: We performed comparative analyses of virtual 3D histology using computed tomography (CT) and conventional 2D histology. For 3D histology we established a contrasting agent-based preparation protocol tailored for delicate underwater plant tissues. KEY RESULTS: Our analyses reveal new structural insights into the adaptive architecture of the complex A. vesiculosa snap-trap. In particular, we discuss in detail the arrangement of sensitive trigger hairs inside the trap and present actual 3D representations of traps with prey. In addition, we provide trap volume calculations at different narrowing stages. Furthermore, the motile zone close to the trap midrib, which is thought to promote not only the fast trap closure by hydraulics but also the subsequent trap narrowing and trap reopening, is described and discussed for the first time in its entirety. CONCLUSIONS: Our research contributes to the understanding of a complex, fast and reversible underwater plant movement and supplements preparation protocols for CT analyses of other non-lignified and sensitive plant structures.

Anaesthesia with diethyl ether impairs jasmonate signalling in the carnivorous plant Venus flytrap (Dionaea muscipula).

BACKGROUND AND AIMS: General anaesthetics are compounds that induce loss of responsiveness to environmental stimuli in animals and humans. The primary site of action of general anaesthetics is the nervous system, where anaesthetics inhibit neuronal transmission. Although plants do not have neurons, they generate electrical signals in response to biotic and abiotic stresses. Here, we investigated the effect of the general volatile anaesthetic diethyl ether on the ability to sense potential prey or herbivore attacks in the carnivorous plant Venus flytrap (Dionaea muscipula). METHODS: We monitored trap movement, electrical signalling, phytohormone accumulation and gene expression in response to the mechanical stimulation of trigger hairs and wounding under diethyl ether treatment. KEY RESULTS: Diethyl ether completely inhibited the generation of action potentials and trap closing reactions, which were easily and rapidly restored when the anaesthetic was removed. Diethyl ether also inhibited the later response: jasmonic acid (JA) accumulation and expression of JA-responsive genes (cysteine protease dionain and type I chitinase). However, external application of JA bypassed the inhibited action potentials and restored gene expression under diethyl ether anaesthesia, indicating that downstream reactions from JA are not inhibited. CONCLUSIONS: The Venus flytrap cannot sense prey or a herbivore attack under diethyl ether treatment caused by inhibited action potentials, and the JA signalling pathway as a consequence.

4D pine scale: biomimetic 4D printed autonomous scale and flap structures capable of multi-phase movement.

We developed biomimetic hygro-responsive composite polymer scales inspired by the reversible shape-changes of Bhutan pine (Pinus wallichiana) cone seed scales. The synthetic kinematic response is made possible through novel four-dimensional (4D) printing techniques with anisotropic material use, namely copolymers with embedded cellulose fibrils and ABS polymer. Multi-phase motion like the subsequent transversal and longitudinal bending deformation during desiccation of a natural pinecone scale can be structurally programmed into such printed hygromorphs. Both the natural concept generator (Bhutan pinecone scale) and the biomimetic technical structure (4D printed scale) were comparatively investigated as to their displacement and strain over time via three-dimensional digital image correlation methods. Our bioinspired prototypes can be the basis for tailored autonomous and self-sufficient flap and scale structures performing complex consecutive motions for technical applications, e.g. in architecture and soft robotics. This article is part of the theme issue 'Bioinspired materials and surfaces for green science and technology (part 3)'.

How the carnivorous waterwheel plant (Aldrovanda vesiculosa) snaps.

The fast motion of the snap-traps of the terrestrial Venus flytrap (Dionaea muscipula) have been intensively studied, in contrast to the tenfold faster underwater snap-traps of its phylogenetic sister, the waterwheel plant (Aldrovanda vesiculosa). Based on biomechanical and functional-morphological analyses and on a reverse biomimetic approach via mechanical modelling and computer simulations, we identify a combination of hydraulic turgor change and the release of prestress stored in the trap as essential for actuation. Our study is the first to identify and analyse in detail the motion principle of Aldrovanda, which not only leads to a deepened understanding of fast plant movements in general, but also contributes to the question of how snap-traps may have evolved and also allows for the development of novel biomimetic compliant mechanisms.

Plant 'muscles': fibers with a tertiary cell wall.

Plants, although sessile organisms, are nonetheless able to move their body parts; for example, during root contraction of geophytes or in the gravitropic reaction by woody stems. One of the major mechanisms enabling these movements is the development of specialized structures that possess contractile properties. Quite unlike animal muscles, for which the action is driven by protein-protein interactions in the protoplasma, the action of plant 'muscles' is polysaccharide-based and located in the uniquely designed, highly cellulosic cell wall that is deposited specifically in fibers. This review describes the development of such cell walls as a widespread phenomenon in the plant kingdom, gives reasons why it should be considered as a tertiary cell wall, and discusses the mechanism of action of the 'muscles'. The origin of the contractile properties lies in the tension of the axially oriented cellulose microfibrils due to entrapment of rhamnogalacturonan-I aggregates that limits the lateral interaction of microfibrils. Long side chains of the nascent rhamnogalacturonan-I are trimmed off during cell wall maturation leading to tension development. Similarities in the tertiary cell wall design in fibers of different plant origin indicate that the basic principles of tension creation may be universal in various ecophysiological situations.

Mechanism for rapid passive-dynamic prey capture in a pitcher plant.

Plants use rapid movements to disperse seed, spores, or pollen and catch animal prey. Most rapid-release mechanisms only work once and, if repeatable, regaining the prerelease state is a slow and costly process. We present an encompassing mechanism for a rapid, repeatable, passive-dynamic motion used by a carnivorous pitcher plant to catch prey. Nepenthes gracilis uses the impact of rain drops to catapult insects from the underside of the canopy-like pitcher lid into the fluid-filled trap below. High-speed video and laser vibrometry revealed that the lid acts as a torsional spring system, driven by rain drops. During the initial downstroke, the tip of the lid reached peak velocities similar to fast animal motions and an order of magnitude faster than the snap traps of Venus flytraps and catapulting tentacles of the sundew Drosera glanduligera. In contrast to these active movements, the N. gracilis lid oscillation requires neither mechanical preloading nor metabolic energy, and its repeatability is only limited by the intensity and duration of rainfall. The underside of the lid is coated with friction-reducing wax crystals, making insects more vulnerable to perturbations. We show that the trapping success of N. gracilis relies on the combination of material stiffness adapted for momentum transfer and the antiadhesive properties of the wax crystal surface. The impact-driven oscillation of the N. gracilis lid represents a new kind of rapid plant movement with adaptive function. Our findings establish the existence of a continuum between active and passive trapping mechanisms in carnivorous plants.

Phototropic solar tracking in sunflower plants: an integrative perspective.

BACKGROUND: One of the best-known plant movements, phototropic solar tracking in sunflower (Helianthus annuus), has not yet been fully characterized. Two questions are still a matter of debate. (1) Is the adaptive significance solely an optimization of photosynthesis via the exposure of the leaves to the sun? (2) Is shade avoidance involved in this process? In this study, these concepts are discussed from a historical perspective and novel insights are provided. SCOPE AND METHODS: Results from the primary literature on heliotropic growth movements led to the conclusion that these responses cease before anthesis, so that the flowering heads point to the East. Based on observations on 10-week-old plants, the diurnal East-West oscillations of the upper fifth of the growing stem and leaves in relation to the position of the sun (inclusive of nocturnal re-orientation) were documented, and photon fluence rates on the leaf surfaces on clear, cloudy and rainy days were determined. In addition, the light-response curve of net CO2 assimilation was determined on the upper leaves of the same batch of plants, and evidence for the occurrence of shade-avoidance responses in growing sunflower plants is summarized. CONCLUSIONS: Only elongating, vegetative sunflower shoots and the upper leaves perform phototropic solar tracking. Photon fluence response and CO2 assimilation measurements cast doubt on the 'photosynthesis-optimization hypothesis' as the sole explanation for the evolution of these plant movements. We suggest that the shade-avoidance response, which maximizes light-driven CO2 assimilation, plays a major role in solar tracking populations of competing sunflower plants, and an integrative scheme of these growth movements is provided.

Artificial and biological supports are different for pea plants.

Previous studies on the kinematics of pea plants' ascent and attach behavior have demonstrated that the signature of their movement varies depending on the kind of support. So far, these studies have been confined to artificial supports (e.g. wooden sticks). Little is known regarding the conditions under which pea plants could rely on biological supports (e.g. neighboring plants) for climbing toward the light. In this study, we capitalize on the 3D kinematic analysis of movement to ascertain whether pea plants scale their kinematics differently depending on whether they aim for artificial or biological support. Results suggest that biological support determines a smoother and more accurate behavior than that elicited by the artificial one. These results shed light on pea plants' ability to detect and classify the properties of objects and implement a movement plan attuned to the very nature of the support. We contend that such differences depend on the augmented multisensory experience elicited by the biological support.

Classifying Circumnutation in Pea Plants via Supervised Machine Learning.

Climbing plants require an external support to grow vertically and enhance light acquisition. Climbers that find a suitable support demonstrate greater performance and fitness than those that remain prostrate. Support search is characterized by oscillatory movements (i.e., circumnutation), in which plants rotate around a central axis during their growth. Numerous studies have elucidated the mechanistic details of circumnutation, but how this phenomenon is controlled during support searching remains unclear. To fill this gap, here we tested whether simulation-based machine learning methods can capture differences in movement patterns nested in actual kinematical data. We compared machine learning classifiers with the aim of generating models that learn to discriminate between circumnutation patterns related to the presence/absence of a support in the environment. Results indicate that there is a difference in the pattern of circumnutation, depending on the presence of a support, that can be learned and classified rather accurately. We also identify distinctive kinematic features at the level of the junction underneath the tendrils that seems to be a superior indicator for discerning the presence/absence of the support by the plant. Overall, machine learning approaches appear to be powerful tools for understanding the movement of plants.

A deep learning approach to track Arabidopsis seedlings' circumnutation from time-lapse videos.

BACKGROUND: Circumnutation (Darwin et al., Sci Rep 10(1):1-13, 2000) is the side-to-side movement common among growing plant appendages but the purpose of circumnutation is not always clear. Accurately tracking and quantifying circumnutation can help researchers to better study its underlying purpose. RESULTS: In this paper, a deep learning-based model is proposed to track the circumnutating flowering apices in the plant Arabidopsis thaliana from time-lapse videos. By utilizing U-Net to segment the apex, and combining it with the model update mechanism, pre- and post- processing steps, the proposed model significantly improves the tracking time and accuracy over other baseline tracking methods. Additionally, we evaluate the computational complexity of the proposed model and further develop a method to accelerate the inference speed of the model. The fast algorithm can track the apices in real-time on a computer without a dedicated GPU. CONCLUSION: We demonstrate that the accuracy of tracking the flowering apices in the plant Arabidopsis thaliana can be improved with our proposed deep learning-based model in terms of both the racking success rate and the tracking error. We also show that the improvement in the tracking accuracy is statistically significant. The time-lapse video dataset of Arabidopsis is also provided which can be used for future studies on Arabidopsis in various takes.

Decision-Making Underlying Support-Searching in Pea Plants.

Finding a suitable support is a key process in the life history of climbing plants. Those that find a suitable support have greater performance and fitness than those that remain prostrate. Numerous studies on climbing plant behavior have elucidated the mechanistic details of support-searching and attachment. Far fewer studies have addressed the ecological significance of support-searching behavior and the factors that affect it. Among these, the diameter of supports influences their suitability. When the support diameter increases beyond some point, climbing plants are unable to maintain tensional forces and therefore lose attachment to the trellis. Here, we further investigate this issue by placing pea plants (Pisum sativum L.) in the situation of choosing between supports of different diameters while their movement was recorded by means of a three-dimensional motion analysis system. The results indicate that the way pea plants move can vary depending on whether they are presented with one or two potential supports. Furthermore, when presented with a choice between thin and thick supports, the plants showed a distinct preference for the former than the latter. The present findings shed further light on how climbing plants make decisions regarding support-searching and provide evidence that plants adopt one of several alternative plastic responses in a way that optimally corresponds to environmental scenarios.

The cracking of Scots pine (Pinus sylvestris) cones.

Pine cones show functionally highly resilient, hygroscopically actuated opening and closing movements, which are repeatable and function even in millions of years old, coalified cones. Although the functional morphology and biomechanics behind the individual seed scale motions are well understood, the initial opening of the cone, which is often accompanied by an audible cracking noise, is not. We therefore investigated the initial opening events of mature fresh cones of Scots pine (Pinus sylvestris) and their subsequent motion patterns. Using high-speed and time lapse videography, 3D digital image correlation techniques, force measurements, thermographic and chemical-rheological resin analyses, we are able to draw a holistic picture of the initial opening process involving the rupture of resin seals and very fast seed scale motion in the millisecond regime. The rapid cone opening was not accompanied by immediate seed release in our experiments and, therefore, cannot be assigned to ballistochory. As the involved passive hydraulic-elastic processes in cracking are very fine-tuned, we hypothesize that they are under tight mechanical-structural control to ensure an ecologically optimized seed release upon environmental conditions suitable for wind dispersal. In this context, we propose an interplay of humidity and temperature to be the external "drivers" for the initial cone opening, in which resin works as a crucial chemical-mechanical latch system.