Robin Seidel

Mechanics without Muscle: Biomechanical Inspiration from the Plant World

Plant and animal biomechanists have much in common. Although their frame of reference differs, they think about the natural world in similar ways. While researchers studying animals might explore airflow around flapping wings, the actuation of muscles in arms and legs, or the material properties of spider silk, researchers studying plants might explore the flow of water around fluttering seaweeds, the grasping ability of climbing vines, or the material properties of wood. Here we summarize recent studies of plant biomechanics highlighting several current research themes in the field: expulsion of high-speed reproductive projectiles, generation of slow movements by shrinking and swelling cell walls, effects of ontogenetic shifts in mechanical properties of stems, flexible reconfiguration and material properties of seaweeds under crashing waves, and the development of botanically-inspired commercial products. Our hope is that this synopsis will resonate with both plant and animal biologists, encourage cross-pollination across disciplines, and promote fruitful interdisciplinary collaborations in the future.

The attachment strategy of English ivy: a complex mechanism acting on several hierarchical levels

English ivy (Hedera helix L.) is able to grow on vertical substrates such as trees, rocks and house plaster, thereby attaching so firmly to the surface that when removed by force typically whole pieces of the climbing substrate are torn off. The structural details of the attachment process are not yet entirely understood. We studied the attachment process of English ivy in detail and suggest a four-phase process to describe the attachment strategy: (i) initial physical contact, (ii) form closure of the root with the substrate, (iii) chemical adhesion, and (iv) shape changes of the root hairs and form-closure with the substrate. These four phases and their variations play an important role in the attachment to differently structured surfaces. We demonstrate that, in English ivy, different mechanisms work together to allow the plants attachment to various climbing substrates and reveal the importance of micro-fibril orientation in the root hairs for the attachment based on structural changes at the subcellular level.

Structure-function relationship of the foam-like pomelo peel (Citrus maxima)-an inspiration for the development of biomimetic damping materials with high energy dissipation.

The mechanical properties of artificial foams are mainly determined by the choice of bulk materials and relative density. In natural foams, in contrast, variation to optimize properties is achieved by structural optimization rather than by conscious substitution of bulk materials. Pomelos (Citrus maxima) have a thick foam-like peel which is capable of dissipating considerable amounts of kinetic energy and thus this fruit represents an ideal role model for the development of biomimetic impact damping structures. This paper focuses on the analysis of the biomechanics of the pomelo peel and on its structure-function relationship. It deals with the determination of the onset strain of densification of this foam-like tissue and on how this property is influenced by the arrangement of vascular bundles. It was found here that the vascular bundles branch in a very regular manner-every 16.5% of the radial peel thickness-and that the surrounding peel tissue (pericarp) attains its exceptional thickness mainly by the expansion of existing interconnected cells causing an increasing volume of the intercellular space, rather than by cell division. These findings lead to the discussion of the pomelo peel as an inspiration for fibre-reinforced cast metallic foams with the capacity for excellent energy dissipation.

Plant surfaces with cuticular folds are slippery for beetles

Plant surfaces covered with three-dimensional (3D) waxes are known to strongly reduce insect adhesion, leading to slippery surfaces. Besides 3D epicuticular waxes, cuticular folds are a common microstructure found on plant surfaces, which have not been quantitatively investigated with regard to their influence on insect adhesion. We performed traction experiments with Colorado potato beetles on five plant surfaces with cuticular folds of different magnitude. For comparison, we also tested (i) smooth plant surfaces and (ii) plant surfaces possessing 3D epicuticular waxes. Traction forces on surfaces with medium cuticular folds, of about 0.5 µm in both height and thickness and a spacing of 0.5–1.5 µm, were reduced by an average of 88 per cent in comparison to smooth plant surfaces. Traction forces were reduced by the same order of magnitude as on plant surfaces covered with 3D epicuticular waxes. For surface characterization, we performed static contact angle measurements, which proved a strong effect of cuticular folds also on surface wettability. Surfaces possessing cuticular folds of greater magnitude showed higher contact angles up to superhydrophobicity. We hypothesize that cuticular folds reduce insect adhesion mainly due to a critical roughness, reducing the real contact area between the surface and the insects adhesive devices.

Morphological aspects of self-repair of lesions caused by internal growth stresses in stems of Aristolochia macrophylla and Aristolochia ringens

This study reveals in detail the mechanism of self-repair during secondary growth in the vines Aristolochia macrophylla and Aristolochia ringens based on morphological data. For a comprehensive understanding of the underlying mechanisms during the self-repair of lesions in the sclerenchymatous cylinder of the stem, which are caused by internal growth stresses, a classification of morphological changes in the cells involved in the repair process is required. In an early stage of self-repair, we observed morphological changes as a mere extension of the turgescent cortex cells surrounding the lesion, whereby the cell wall extends locally through visco-elastic/plastic deformation without observable cell wall synthesis. Later stages involve typical cell growth and cell division. Several successive phases of self-repair were investigated by light microscopy of stained samples and confocal laser-scanning microscopy in fluorescence mode. The results indicate that A. macrophylla and A. ringens respond to lesions caused by internal growth stresses with a sophisticated self-repair mechanism comprising several phases of different repair modes.

Temporal Tissue Patterns in Bone Healing of Sheep

Secondary fracture healing in long bones leads to the successive formation of intricate patterns of tissues in the newly formed callus. The main aim of this work was to quantitatively describe the topology of these tissue patterns at different stages of the healing process and to generate averaged images of tissue distribution. This averaging procedure was based on stained histological sections (2, 3, 6, and 9 weeks post‐operatively) of 64 sheep with a 3 mm tibial mid‐shaft osteotomy, stabilized either with a rigid or a semi‐rigid external fixator. Before averaging, histological images were sorted for topology according to six identified tissue patterns. The averaged images were obtained for both fixation types and the lateral and medial side separately. For each case, the result of the averaging procedure was a collection of six images characterizing quantitatively the progression of the healing process. In addition, quantified descriptions of the newly formed cartilage and the bone area fractions (BA/TA) of the bony callus are presented. For all cases, a linear increase in the BA/TA of the bony callus was observed. The slope was greatest in the case of the most rigid stabilization and lowest in the case of the least stiff. This topological description of the progression of bone healing will allow quantitative validation (or falsification) of current mechano‐biological theories.

Catapulting Tentacles in a Sticky Carnivorous Plant

Among trapping mechanisms in carnivorous plants, those termed ‘active’ have especially fascinated scientists since Charles Darwin’s early works because trap movements are involved. Fast snap-trapping and suction of prey are two of the most spectacular examples for how these plants actively catch animals, mainly arthropods, for a substantial nutrient supply. We show that Drosera glanduligera, a sundew from southern Australia, features a sophisticated catapult mechanism: Prey animals walking near the edge of the sundew trigger a touch-sensitive snap-tentacle, which swiftly catapults them onto adjacent sticky glue-tentacles; the insects are then slowly drawn within the concave trap leaf by sticky tentacles. This is the first detailed documentation and analysis of such catapult-flypaper traps in action and highlights a unique and surprisingly complex mechanical adaptation to carnivory.

Plant surfaces with cuticular folds and their replicas: Influence of microstructuring and surface chemistry on the attachment of a leaf beetle

Plant surfaces covered either with epicuticular wax crystals or cuticular folds have been shown to strongly reduce the ability of insects to attach to them. However, the relative impact of surface structuring vs. surface chemistry on insect attachment remains unclear. To understand the mechanisms reducing adhesion of insects on plant surfaces in more detail, we performed traction experiments (i) on plant surfaces covered with cuticular folds of different dimensions, and on their (ii) untreated and (iii) hydrophobized replicas. As a reference, measurements were performed on replicas of smooth plant surfaces and of glass. Traction forces were measured with a highly sensitive force transducer, using tethered male Colorado potato beetles (Leptinotarsa decemlineata) as a model insect species. Contact angle measurements with water and diiodomethane were also performed to examine the physicochemical properties of the test surfaces. We found that surface structuring has a strong influence on the magnitude of the attachment force. In contrast, under the chosen experimental conditions, surface chemistry had no significant influence. Our results indicate that attachment of the beetles is reduced solely by the dimensions of the folds, with cuticular folds of about 0.5 μm in both height and width being the most effective. Contrary to the attachment of beetles, the wettability of the surfaces was considerably influenced by both surface structuring and chemistry. These results contribute to a better understanding of plant-insect interactions and the function of microstructured surfaces, and may facilitate the development of biomimetic anti-adhesive surfaces.

Impact of cell shape in hierarchically structured plant surfaces on the attachment of male Colorado potato beetles (Leptinotarsa decemlineata)

Summary Plant surfaces showing hierarchical structuring are frequently found in plant organs such as leaves, petals, fruits and stems. In our study we focus on the level of cell shape and on the level of superimposed microstructuring, leading to hierarchical surfaces if both levels are present. While it has been shown that epicuticular wax crystals and cuticular folds strongly reduce insect attachment, and that smooth papillate epidermal cells in petals improve the grip of pollinators, the impact of hierarchical surface structuring of plant surfaces possessing convex or papillate cells on insect attachment remains unclear. We performed traction experiments with male Colorado potato beetles on nine different plant surfaces with different structures. The selected plant surfaces showed epidermal cells with either tabular, convex or papillate cell shape, covered either with flat films of wax, epicuticular wax crystals or with cuticular folds. On surfaces possessing either superimposed wax crystals or cuticular folds we found traction forces to be almost one order of magnitude lower than on surfaces covered only with flat films of wax. Independent of superimposed microstructures we found that convex and papillate epidermal cell shapes slightly enhance the attachment ability of the beetles. Thus, in plant surfaces, cell shape and superimposed microstructuring yield contrary effects on the attachment of the Colorado potato beetle, with convex or papillate cells enhancing attachment and both wax crystals or cuticular folds reducing attachment. However, the overall magnitude of traction force mainly depends on the presence or absence of superimposed microstructuring.

Structure, attachment properties, and ecological importance of the attachment system of English ivy (Hedera helix)

Root climbers such as English ivy (Hedera helix) rely on specialized adventitious roots for attachment, enabling the plants to climb on a wide range of natural and artificial substrates. Despite their importance for the climbing habit, the biomechanical properties of these specialized adventitious roots compared with standard roots and their performance in the attachment to different host species or inert substrates have not been studied. Here organs and tissues involved in the attachment are characterized and their significance in regard to a broader functional and ecological aspect is discussed. Depending on the substrate, the root clusters show different types of failure modes at various frequencies, demonstrating the close interaction between the climber and its substrates. With a Young’s Modulus of 109.2 MPa, the attachment roots are relatively stiff for non-woody roots. The central cylinders of the attachment roots show a high tensile strength of 38 MPa and a very high extensibility of 34%. In host trees naturally co-distributed with English ivy, a ‘balanced’ occurrence of failure of the attachment system of the climber and the bark of the host is found, suggesting a co-evolution of climber and host. Maximum loads of root clusters normalized by the number of roots match those of individually tested attachment roots. In comparison with most subterranean roots the properties and structure of the attachment roots of English ivy show distinct differences. There exist similarities to the properties found for roots of Galium aparine, suggesting a trend in not fully self-supporting plants towards a higher extensibility.