Natural coil springs: Biomechanics and morphology of the coiled tendrils of the climbing passion flower Passiflora discophora.

Tendrils of climbing plants possess a striking spring-like structure characterized by a minimum of two helices of opposite handedness connected by a perversion. By performing tensile experiments and morphological measurements on tendrils of the climbing passion flower Passiflora discophora, we show that these tendril springs act as coil springs within the plant's attachment system and resemble technical coil springs. However, tendril springs have a low spring index and a high pitch angle compared with typical metal coil springs resulting in a more complex loading situation in the plant tendrils. Moreover, the tendrils undergo a drastic shift from the fresh turgescent stage to a dried-off and dead senescent stage. This entails changes in material properties (elastic modulus in tension), morphology (tendril and helix diameter, number of windings), anatomy (tissue composition), and failure behavior (susceptibility to delamination) and reduces the degree of elasticity and strain at failure of the tendrils. Nevertheless, senescent tendrils remain functional as springs and maintain high energy dissipation capacity and high break force. This renders the system highly energy efficient, as the plant no longer needs to metabolically sustain the died-back tendrils. Because of its energy-storing spring system, its high energy dissipation and high safety factor, the attachment system can be considered a 'fail-safe' system. STATEMENT OF SIGNIFICANCE: The use of coil springs as mechanical devices is not restricted to man-made machinery; striking spring structures can also be found within the attachment systems of climbing plants. Passiflora discophora climbs by using long thin tendrils with adhesive pads at their tips. Once the pads have attached to a support, the tendrils coil and form a spring-like structure. Here, we analyze the form and mechanics of these 'tendril springs', compare them with conventional technical coil springs, and discuss changes in the tendril springs during plant development. We reveal the main features of the attachment system, which might inspire new artificial attachment devices within the emerging field of plant-inspired soft-robotics.

Force Generation in the Coiling Tendrils of Passiflora caerulea.

Tendrils of climbing plants coil along their length, thus forming a striking helical spring and generating tensional forces. It is found that, for tendrils of the passion flower Passiflora caerulea, the generated force lies in the range of 6-140 mN, which is sufficient to lash the plant tightly to its substrate. Further, it is revealed that the generated force strongly correlates with the water status of the plant. Based on a combination of in situ force measurements with anatomical investigations and dehydration-rehydration experiments on both entire tendril segments and isolated lignified tissues, a two-phasic mechanism for spring formation is proposed. First, during the free coiling phase, the center of the tendril begins to lignify unilaterally. At this stage, both the generated tension and the stability of the form of the spring still depend on turgor pressure. The unilateral contraction of a bilayer as being the possible driving force for the tendril coiling motion is discussed. Second, in a stabilization phase, the entire center of the coiled tendril lignifies, stiffening the spring and securing its function irrespective of its hydration status.

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.

Artificial Tendrils Mimicking Plant Movements by Mismatching Modulus and Strain in Core and Shell.

Motile organs have evolved in climbing plants enabling them to find a support and, after secure attachment, to reach for sunlight without investing in a self-supporting stem. Searching movements, the twining of stems, and the coiling of tendrils are involved in successful plant attachment. Such coiling movements have great potential in robotic applications, especially if they are reversible. Here, the underlying mechanism of tendril movement based on contractile fibers is reported, as illustrated by a function-morphological analysis of tendrils in several liana species and the encoding of such a principle in a core-shell multimaterial fiber (MMF) system. MMFs are composed of a shape-memory core fiber (SMCF) and an elastic shell. The shape-memory effect of the core fibers enables the implementation of strain mismatch in the MMF by physical means and provides thermally controlled reversible motion. The produced MMFs show coiling and/or uncoiling behavior, with a high reversible actuation magnitude of ≈400%, which is almost 20 times higher compared with similar stimuli for sensitive soft actuators. The movements in these MMFs rely on the crystallization/melting behavior of oriented macromolecules of SMCF.

Improvement of a microfiber filter for domestic washing machines.

The development of enhanced processes for filtration is one solution for stopping the increasing freshwater and sea pollution caused by microplastic and microfibers. Major contributors to micro-X pollution are domestic devices such as washing machines, which also hold a high technical potential for separating problematic soils from waste water during cleaning cycles. The focus of the present paper are the biomimetic development of a novel concept for filtration and removal of particles such as microfibers in conventional washing machines. To this goal, a TRIZ analysis yielded viable solutions for the major key issues. In a next step, measurements were made with various filters with and without ribbed structures. The results are promising for the incorporation in a filter concept that is easy to operate and cost-effective.

Functional Anatomy, Impact Behavior and Energy Dissipation of the Peel of Citrus × limon: A Comparison of Citrus × limon and Citrus maxima.

This study analyzes the impact behavior of lemon peel (Citrus × limon) and investigates its functional morphology compared with the anatomy of pomelo peel (Citrusmaxima). Both fruit peels consist mainly of parenchyma structured by a density gradient. In order to characterize the lemon peel, both energy dissipation and transmitted force are determined by conducting drop weight tests at different impact strengths (0.15-0.74 J). Fresh and freeze-dried samples were used to investigate the influence on the mechanics of peel tissue's water content. The samples of lemon peel dissipate significantly more kinetic energy in the freeze-dried state than in the fresh state. Fresh lemon samples experience a higher impulse than freeze-dried samples at the same momentum. Drop weight tests results show that fresh lemon samples have a significantly longer impact duration and lower transmitted force than freeze-dried samples. With higher impact energy (0.74 J) the impact behavior becomes more plastic, and a greater fraction of the kinetic energy is dissipated. Lemon peel has pronounced energy dissipation properties, even though the peel is relatively thin and lemon fruits are comparably light. The cell arrangement of citrus peel tissue can serve as a model for bio-inspired, functional graded materials in technical foams with high energy dissipation.

Biomechanics of tendrils and adhesive pads of the climbing passion flower Passiflora discophora.

The climbing passion flower Passiflora discophora features branched tendrils with multiple adhesive pads at their tips allowing it to attach to large-diameter supports and to flat surfaces. We conducted tensile tests to quantify the performance of this attachment system. We found that the force at failure varies with substrate, ontogenetic state (turgescent or senescent), and tendril size (i.e. tendril cross-sectional area and pad area). The tendrils proved to be well balanced in size and to attach firmly to a variety of substrates (force at failure up to 2N). Pull-off tests performed with tendrils grown on either epoxy, plywood, or beech bark revealed that senescent tendrils could still bear 24, 64, or 100% of the force measured for turgescent tendrils, respectively, thus providing long-lasting attachment at minimal physiological costs. The tendril main axis was typically the weakest part of the adhesive system, whereas the pad-substrate interface never failed. This suggests that the plants use the slight oversizing of adhesive pads as a strategy to cope with 'unpredictable' substrates. The pads, together with the spring-like main axis, which can, as shown, dissipate a large amount of energy when straightened, thus constitute a fail-safe attachment system.

Polarity in cuticular ridge development and insect attachment on leaf surfaces of Schismatoglottis calyptrata (Araceae).

The plant cuticle is a multifunctional barrier that separates the organs of the plant from the surrounding environment. Cuticular ridges are microscale wrinkle-like cuticular protrusions that occur on many flower and leaf surfaces. These microscopic ridges can help against pest insects by reducing the frictional forces experienced when they walk on the leaves and might also provide mechanical stability to the growing plant organs. Here, we have studied the development of cuticular ridges on adaxial leaf surfaces of the tropical Araceae Schismatoglottis calyptrata. We used polymer replicas of adaxial leaf surfaces at various ontogenetic stages to study the morphological changes occurring on the leaf surfaces. We characterized the replica surfaces by using confocal laser scanning microscopy and commercial surface analysis software. The development of cuticular ridges is polar and the ridge progression occurs basipetally with a specific inclination to the midrib on Schismatoglottis calyptrata leaves. Using Colorado potato beetles as model species, we performed traction experiments on freshly unrolled and adult leaves and found low walking frictional forces of insects on both of these surfaces. The changes in the micro- and macroscale morphology of the leaves should improve our understanding of the way that plants defend themselves against insect herbivores.

Jumping with adhesion: landing surface incline alters impact force and body kinematics in crested geckos.

Arboreal habitats are characterized by a complex three-dimensional array of branches that vary in numerous characteristics, including incline, compliance, roughness, and diameter. Gaps must often be crossed, and this is frequently accomplished by leaping. Geckos bearing an adhesive system often jump in arboreal habitats, although few studies have examined their jumping biomechanics. We investigated the biomechanics of landing on smooth surfaces in crested geckos, Correlophus ciliatus, asking whether the incline of the landing platform alters impact forces and mid-air body movements. Using high-speed videography, we examined jumps from a horizontal take-off platform to horizontal, 45° and 90° landing platforms. Take-off velocity was greatest when geckos were jumping to a horizontal platform. Geckos did not modulate their body orientation in the air. Body curvature during landing, and landing duration, were greatest on the vertical platform. Together, these significantly reduced the impact force on the vertical platform. When landing on a smooth vertical surface, the geckos must engage the adhesive system to prevent slipping and falling. In contrast, landing on a horizontal surface requires no adhesion, but incurs high impact forces. Despite a lack of mid-air modulation, geckos appear robust to changing landing conditions.

Biohybrid generators based on living plants and artificial leaves: influence of leaf motion and real wind outdoor energy harvesting.

Plants translate wind energy into leaf fluttering and branch motion by reversible tissue deformation. Simultaneously, the outermost structure of the plant, i.e. the dielectric cuticula, and the inner ion-conductive tissue can be used to convert mechanical vibration energy, such as that produced during fluttering in the wind, into electricity by surface contact electrification and electrostatic induction. Constraining a tailored artificial leaf to a plant leaf can enhance oscillations and transient mechanical contacts and thereby increase the electricity outcome. We have studied the effects of wind-induced mechanical interactions between the leaf of a plant (Rhododendron) and a flexible silicone elastomer-based artificial leaf fixed at the petiole on power output and whether performance can be further tuned by altering the vibrational behavior of the artificial leaf. The latter is achieved by modifying a concentrated mass at the tip of the artificial leaf and observing plant-generated current and voltage signals under air flow. In this configuration, the plant-hybrid wind-energy converters can directly power light-emitting diodes and a temperature sensor. Detailed output analysis has revealed that, under all conditions, an increase in wind speed leads to nearly linearly increased voltages and currents. Accordingly, the cumulative sum energy reaches its highest values at the highest wind speed and resulting oscillations of the plant-artificial leaf system. The mass at the tip can, in most cases, be used to increase the voltage amplitude and frequency. Nevertheless, this behavior was found to depend on the individual configuration of the system, such as the leaf morphology. Analysis of these factors under controlled conditions is crucial for optimizing systems meant to operate in unstructured outdoor scenarios. We have established, in a first approach, that the artificial leaf-plant hybrid generator is capable of autonomously generating electricity outdoors under real outdoor wind conditions, even at a low average wind speed of only 1.9 m s-1.

Bio-Inspired Motion Mechanisms: Computational Design and Material Programming of Self-Adjusting 4D-Printed Wearable Systems.

This paper presents a material programming approach for designing 4D-printed self-shaping material systems based on biological role models. Plants have inspired numerous adaptive systems that move without using any operating energy; however, these systems are typically designed and fabricated in the form of simplified bilayers. This work introduces computational design methods for 4D-printing bio-inspired behaviors with compounded mechanisms. To emulate the anisotropic arrangement of motile plant structures, material systems are tailored at the mesoscale using extrusion-based 3D-printing. The methodology is demonstrated by transferring the principle of force generation by a twining plant (Dioscorea bulbifera) to the application of a self-tightening splint. Through the tensioning of its stem helix, D. bulbifera exhibits a squeezing force on its support to provide stability against gravity. The functional strategies of D. bulbifera are abstracted and translated to customized 4D-printed material systems. The squeezing forces of these bio-inspired motion mechanisms are then evaluated. Finally, the function of self-tightening is prototyped in a wrist-forearm splint-a common orthotic device for alignment. The presented approach enables the transfer of novel and expanded biomimetic design strategies to 4D-printed motion mechanisms, further opening the design space to new types of adaptive creations for wearable assistive technologies and beyond.

Searching and Intertwining: Climbing Plants and GrowBots.

Applications in remote inspection and medicine have motivated the recent development of innovative thin, flexible-backboned robots. However, such robots often experience difficulties in maintaining their intended posture under gravitational and other external loadings. Thin-stemmed climbing plants face many of the same problems. One highly effective solution adopted by such plants features the use of tendrils and tendril-like structures, or the intertwining of several individual stems to form braid-like structures. In this paper, we present new plant-inspired robotic tendril-bearing and intertwining stem hardware and corresponding novel attachment strategies for thin continuum robots. These contributions to robotics are motivated by new insights into plant tendril and intertwining mechanics and behavior. The practical applications of the resulting GrowBots is discussed in the context of space exploration and mining operations.

Spatio-temporal development of cuticular ridges on leaf surfaces of Hevea brasiliensis alters insect attachment.

Cuticular ridges on plant surfaces can control insect adhesion and wetting behaviour and might also offer stability to underlying cells during growth. The growth of the plant cuticle and its underlying cells possibly results in changes in the morphology of cuticular ridges and may also affect their function. We present spatial and temporal patterns in cuticular ridge development on the leaf surfaces of the model plant, Hevea brasiliensis. We have identified, by confocal laser scanning microscopy of polymer leaf replicas, an acropetally directed progression of ridges during the ontogeny of Hevea brasiliensis leaf surfaces. The use of Colorado potato beetles (Leptinotarsa decemlineata) as a model insect species has shown that the changing dimensions of cuticular ridges on plant leaves during ontogeny have a significant impact on insect traction forces and act as an effective indirect defence mechanism. The traction forces of walking insects are significantly lower on mature leaf surfaces compared with young leaf surfaces. The measured walking traction forces exhibit a strong negative correlation with the dimensions of the cuticular ridges.

Replicating the complexity of natural surfaces: technique validation and applications for biomimetics, ecology and evolution.

The surfaces of animals, plants and abiotic structures are not only important for organismal survival, but they have also inspired countless biomimetic and industrial applications. Additionally, the surfaces of animals and plants exhibit an unprecedented level of diversity, and animals often move on the surface of plants. Replicating these surfaces offers a number of advantages, such as preserving a surface that is likely to degrade over time, controlling for non-structural aspects of surfaces, such as compliance and chemistry, and being able to produce large areas of a small surface. In this paper, we compare three replication techniques among a number of species of plants, a technical surface and a rock. We then use two model parameters (cross-covariance function ratio and relative topography difference) to develop a unique method for quantitatively evaluating the quality of the replication. Finally, we outline future directions that can employ highly accurate surface replications, including ecological and evolutionary studies, biomechanical experiments, industrial applications and improving haptic properties of bioinspired surfaces. The recent advances associated with surface replication and imaging technology have formed a foundation on which to incorporate surface information into biological sciences and to improve industrial and biomimetic applications. This article is part of the theme issue 'Bioinspired materials and surfaces for green science and technology'.

Impact behaviour of freeze-dried and fresh pomelo (Citrus maxima) peel: influence of the hydration state.

Pomelos (Citrus maxima) are known for their thick peel which-inter alia-serves as energy dissipator when fruits impact on the ground after being shed. It protects the fruit from splitting open and thus enables the contained seeds to stay germinable and to potentially be dispersed by animal vectors. The main part of the peel consists of a parenchymatous tissue that can be interpreted from a materials point of view as open pored foam whose struts are pressurized and filled with liquid. In order to investigate the influence of the water content on the energy dissipation capacity, drop weight tests were conducted with fresh and with freeze-dried peel samples. Based on the coefficient of restitution it was found that freeze-drying markedly reduces the relative energy dissipation capacity of the peel. Measuring the transmitted force during impact furthermore indicated a transition from a uniform collapse of the foam-like tissue to a progressive collapse due to water extraction. Representing the peel by a Maxwell model illustrates that freeze-drying not only drastically reduces the damping function of the dashpots but also stiffens the springs of the model.