Plant latex, the source of natural rubber, has been of interest to mankind for millennia, with much of the research on its rheological (flow) properties focused towards industrial application. However, little is known regarding the rheology of the native material as produced by the plant, a key factor in determining latex's biological functions. In this study, we outline a method for rheological comparison between native latices that requires a minimum of preparatory steps. Our approach provides quantitative insights into the coagulation mechanisms of Euphorbia and Ficus latex allowing interpretation within a comparative evolutionary framework. Our findings reveal that in laboratory conditions both latices behave like non-Newtonian materials with the coagulation of Euphorbia latex being mediated by a slow evaporative process (more than 60 min), whereas Ficus appears to use additional biochemical components to increase the rate of coagulation (more than 30 min). Based on these results, we propose two different primary defensive roles for latex in these plants: the delivery of anti-herbivory compounds (Euphorbia) and rapid wound healing (Ficus).
rheology; latex; Euphorbia; Ficus; evolution; coagulation
Branching in columnar cacti features morphological and anatomical characteristics specific to the subfamily Cactoideae. The most conspicuous features are the pronounced constrictions at the branch–stem junctions, which are also present in the lignified vascular structures within the succulent cortex. Based on finite-element analyses of ramification models, we demonstrate that these indentations in the region of high flexural and torsional stresses are not regions of structural weakness (e.g. allowing vegetative propagation). On the contrary, they can be regarded as anatomical adaptations to increase the stability by fine-tuning the stress state and stress directions in the junction along prevalent fibre directions. Biomimetic adaptations improving the functionality of ramifications in technical components, inspired, in particular, by the fine-tuned geometrical shape and arrangement of lignified strengthening tissues of biological role models, might contribute to the development of alternative concepts for branched fibre-reinforced composite structures within a limited design space.
columnar cacti; functional anatomy; branching; finite-element analysis; biomimetics
Among latex-producing plants, mainly the latex of Hevea brasiliensis has been studied in detail so far, while comprehensive comparative studies of latex coagulation mechanisms among the more than 20,000 latex-bearing plant species are lacking. In order to give new insights into the potential variety of coagulation mechanisms, the untreated natural latices of five latex-bearing plants from the families Euphorbiaceae, Moraceae and Campanulaceae were visualised using Cryo-SEM and their particle size compared using the laser diffraction method. Additionally, the laticifers of these plants species were examined in planta via Cryo-SEM. Similar latex particle sizes and shape were found in Ficus benjamina and Hevea brasiliensis. Hence, and due to other similarities, we hypothesize comparable, mainly chemical, coagulation mechanisms in these two species, whereas a physical coagulation mechanism is proposed for the latex of Euphorbia spp. The latter mechanism is based on the huge amount of densely packed particles that after evaporation of water build a large surface area, which accelerates the coagulation procedure.
The shells/coats of nuts and seeds are often very hard to crack. This is particularly the case with Macadamia seed coats, known to exhibit astoundingly high strength and toughness. We performed an extensive materials science characterization of the complex hierarchical structure of these coats, using light and scanning electron microscopy in 2D as well as microCT for 3D characterization. We differentiate nine hierarchical levels that characterize the structure ranging from the whole fruit on the macroscopic scale down to the molecular scale. From a biological viewpoint, understanding the hierarchical structure may elucidate why it is advantageous for these seed coats to be so difficult to break. From an engineering viewpoint, microstructure characterization is important for identifying features that contribute to the high strength and cracking resistance of these objects. This is essential for revealing the underlying structure-function-relationships. Such information will help us develop engineering materials and lightweight-structures with improved fracture and puncture resistance.
We review trapping mechanisms in the carnivorous flowering plant family Droseraceae (order Caryophyllales). Its members are generally known to attract, capture, retain and digest prey animals (mainly arthropods) with active snap-traps (Aldrovanda, Dionaea) or with active sticky flypaper traps (Drosera) and to absorb the resulting nutrients. Recent investigations revealed how the snap-traps of Aldrovanda vesiculosa (waterwheel plant) and Dionaea muscipula (Venus’ flytrap) work mechanically and how these apparently similar devices differ as to their functional morphology and shutting mechanics. The Sundews (Drosera spp.) are generally known to possess leaves covered with glue-tentacles that both can bend toward and around stuck prey. Recently, it was shown that there exists in this genus a higher diversity of different tentacle types and trap configurations than previously known which presumably reflect adaptations to different prey spectra. Based on these recent findings, we finally comment on possible ways for intrafamiliar trap evolution.
Aldrovanda; carnivorous plant; catapult-flypaper-trap; Dionaea; Drosera; sticky flypaper trap; snap-trap
Background and Aims
The functions of plant latex have been discussed for a long time. Today, many studies support a defence mechanism as being its main function. A role as a self-healing mechanism was never attributed to the coagulation of latex. In this study we quantified the contribution of the coagulation of Ficus benjamina (weeping fig) latex to a restoration of the mechanical properties of the bark after external lesions.
Tensile tests of F. benjamina bark were conducted either immediately after injury or at various latency times after injury.
A significant increase in the tensile strength of bark samples until 30 min after injury was found, and this effect could be attributed to the coagulation of plant latex alone. The tensile strength remains nearly constant until several hours or days after injury. Then, very probably due to other mechanisms such as cell growth and cell proliferation, the tensile strength begins to increase slightly again.
The coagulation of latex seals lesions and serves as a quick and effective pre-step of subsequent, more effective, long-lasting self-healing mechanisms such as cell growth and proliferation. Thus, a fast self-healing effect can be included in the list of functions of plant latex.
Self-healing; latex coagulation; tensile strength; external lesion; Ficus benjamina
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 insect's adhesive devices.
adhesion; attachment; biomimetic surfaces; epicuticular waxes; insect–plant interaction; microstructure
Carnivorous aquatic Utricularia species catch small prey animals using millimetre-sized underwater suction traps, which have fascinated scientists since Darwin's early work on carnivorous plants. Suction takes place after mechanical triggering and is owing to a release of stored elastic energy in the trap body accompanied by a very fast opening and closing of a trapdoor, which otherwise closes the trap entrance watertight. The exceptional trapping speed—far above human visual perception—impeded profound investigations until now. Using high-speed video imaging and special microscopy techniques, we obtained fully time-resolved recordings of the door movement. We found that this unique trapping mechanism conducts suction in less than a millisecond and therefore ranks among the fastest plant movements known. Fluid acceleration reaches very high values, leaving little chance for prey animals to escape. We discovered that the door deformation is morphologically predetermined, and actually performs a buckling/unbuckling process, including a complete trapdoor curvature inversion. This process, which we predict using dynamical simulations and simple theoretical models, is highly reproducible: the traps are autonomously repetitive as they fire spontaneously after 5–20 h and reset actively to their ready-to-catch condition.
bladderwort; carnivorous/insectivorous plants; suction mechanism; functional morphology; fluid dynamics; Utricularia
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.
Galium aparine is a herbaceous climbing plant that attaches to host plants mainly via its leaves, which are covered by hooked trichomes. Although such hooks are found on both leaf surfaces, the leaves of G. aparine are mainly positioned upon the leaves of supporting plants and rarely beneath. In order to understand the mechanism underlying this observation, we have studied structural and mechanical properties of single leaf hooks, frictional properties of leaf surfaces, turgor pressure in different leaf tissues and bending properties of the leaves in different directions. Abaxial and adaxial leaf hooks differ significantly in orientation, distribution, structure and mechanical properties. In accordance with these differences, friction properties of leaves depend on the direction of the applied force and differ significantly between both leaf surfaces. This results in a ratchet mechanism. Abaxial leaf hooks provide strong attachment upon the leaves of adjacent plants, whereas adaxial hooks cause a gliding-off from the underside of the leaves of host plants. Thus, the leaves of G. aparine can function as attachment organs, and simultaneously orient themselves advantageously for their photosynthetic function. Further adaptations in turgor pressure or concerning an anisotropy of the flexural stiffness of the leaves have not been found.
semi-self-supporter; leaf hooks; attachment; mechanical properties; ratchet mechanism
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.
cuticular folds; epicuticular wax crystals; insect–plant interaction; papillae; structure–function relationship
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.
Attachment system; biomechanics; English ivy; Hedera helix; maximum strain; root climber; substrate; tensile strength; Young’s Modulus
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 plant's 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.
attachment system; Hedera helix; root climber; English ivy; form-structure–function; adventitious roots
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.
Aristolochia macrophylla; Aristolochia ringens; self-healing; self-repair; vine; growth stress
Branching in plants is one of the most important assets for developing large arborescent growth forms with complex crowns. While the form and development of branching in gymnosperms and dicotyledonous trees is widely understood, very little is known about branching patterns and the structure of branch–stem-junctions in arborescent monocotyledons. For a better and quantitative understanding of the functional morphology of branch–stem-junctions in arborescent monocotyledons, we investigated the two species Dracaena reflexa and Freycinetia insignis. While D. reflexa is able to develop large arborescent forms with conspicuous crowns by anomalous secondary growth, F. insignis remains relatively small and is only capable of primary growth. Biomechanical investigations were performed by applying vertical loads up to rupture to lateral branches of both species. This allows the analysis of the fracture mechanics and the determination of the maximal force, stress and strain at rupture as well as the fracture toughness. Functional morphology was correlated with the mechanical behaviour of these plants and compared to data of other dicotyledonous trees. The high energy absorption found in the rupture process of lateral branches of D. reflexa and F. insignis makes them promising biological concept generators with a high potential for biomimetic implementation, i.e., for the development of branched fibre-reinforced technical composites. A wide range of constructional elements with branched (sub-)structures can be optimised by using solutions inspired by plant ramifications, e.g., in automotive and aerospace engineering, architecture, sports equipment and prosthetic manufacturing.
Biomimetics; branching; Dracaena reflexa; Freycinetia insignis; monocotyledons
The culms of the giant reed Arundo donax represent slender tube-like structures. Several nodes along the culm, a ring of sclerenchymatous fibres in the periphery of the culm wall and numerous isolated vascular bundles enclosed by fibre rings in the culm wall function as stiffening elements. The bundles are embedded in lignified parenchyma. Micromechanical analysis indicated differences in stiffness between the individual tissues of more than one order of magnitude. In case of abrupt transitions in stiffness at the interfaces, stress discontinuities arise under dynamic loads. This eventually leads to critical shear stresses at cell ends, and culm failure may be initiated at these points. Pronounced mechanical differences between individual tissues can be compromised by gradual transitions at their interfaces. Ultrastructural and spectroscopic investigations with high spatial resolution revealed a gradual transition of cell parameters (cell wall area fraction and cell length). However, cell wall parameters (cellulose microfibril angle and lignin content) showed abrupt transitions or remained almost constant across the interfaces between various tissues. The design principles found at the interfaces between tissues in the culm walls of A. donax are discussed as an adaptation strategy to mechanical loads at different levels of hierarchy.
Arundo donax; micromechanics; stiffness; microfibril angle; hierarchy; gradients
Palms can grow at sites exposed to high winds experiencing large dynamic wind and gust loads. Their stems represent a system of stiff fibrous elements embedded in the soft parenchymatous tissue. The proper design of the interface of the stiffening elements and the parenchyma is crucial for the functioning of the stem. The strategy of the palm to compromise between stiff fibre caps and the soft parenchymatous tissue may serve as a model system for avoiding stress discontinuities in inhomogeneous and anisotropic fibre-reinforced composite materials. We investigated the mechanical, structural and biochemical properties of the fibre caps of the palm Washingtonia robusta at different levels of hierarchy with high spatial resolution. A gradual decrease in stiffness across the fibre cap towards the surrounding parenchymatous tissue was observed. Structural adaptations at the tissue level were found in terms of changes in cell cross sections and cell wall thickness. At the cell wall level, gradients across the fibre cap were found in the degree of orientation of the microfibrils and in the lignin level and composition. The impact of these structural variations in the local material stiffness distribution is discussed.
palms; gradients; micromechanics; tensile stiffness; cell wall; lignin composition
Background and Aims
The functional morphology of Salvia pratensis flowers was re-investigated, after new insights revealed that pollen dispensing is one of the main functions of the staminal lever. In particular, no detailed information was available regarding the process of pollen transfer and the forces arising between the pollen-bearing thecae and the pollinating bee's body. The assumption was made that these forces play a significant role in pollen dispensing.
The functional morphology of S. pratensis flowers and the interaction between flowers and bees (Apis mellifera) were studied by reconstructing stress and strains by using qualitative and semi-quantitative theoretical analysis. Flowers were manipulated to study the spatial arrangement of the filament and lever, and of the head and proboscis of the visiting bee inside the tube. Photographs and films of bee visits on flowers were used to analyse the interaction of pollinator and staminal lever.
The spoon-shaped lower lever of S. pratensis has a small hole through which a bee introduces its proboscis into the corolla tube. Although mentioned for the first time by Kerner von Marilaun in 1891, presented here is the first drawing and the first photograph showing this interaction in detail. The analysis of the interaction of flower visitor and the lever mechanism revealed that the position of bees on different flowers is spatially very similar. Flower morphology constrains postures of legitimately nectar-probing bees within narrow bounds. A theoretical discussion on structural elements and force progression in the flower allows the principles of lightweight architecture in flower morphology to be recognized.
The staminal lever of S. pratensis is a pollen-dispensing device. It seems to influence the amount of pollen deposited on pollinators by determining the forces arising between the pollinator and the pollen. The relevant forces occur either during the first, dynamic phase or during the second, almost static phase of a flower visit.
Flower–pollinator interaction; bee; Apis mellifera; pollination; pollen uptake; see-saw mechanism; biomechanics; pollen dispensing
The anatomy of young and old stems of Aristolochia macrophylla has been investigated for a better understanding of how secondary growth processes cause changes in the stem anatomy of a lianescent plant. In A. macrophylla, following an increase in volume of secondary vascular tissues, the cortical tissues are deformed and the outer sclerenchymatous cylinder ruptures. Morphometric measurements prove that the inner zone of the cortical parenchymatous tissue is compressed prior to the rupture of the outer sclerenchymatous cylinder. After the rupture has occurred, the radial width of the inner primary cortex slightly increases again. This could be caused by strain relaxation, suggesting that the inner primary cortex mechanically behaves similarly to cellular technical foam rubbers. Two different experiments were undertaken to test the outer cortical cylinders mechanically. The outer cortical cylinders comprise the outer sclerenchymatous cortical tissue and a collenchymatous sheath underneath the epidermis and the epidermis. In a first experiment, transverse compression loads were applied to the outside of the cortical cylinders causing ovalization of the cylinder until failure. This experiment allowed the Young's Modulus of the outer cortical cylinders to be determined. In a second set of experiments, radial hydraulic pressure was applied to the inside of the cortical cylinders, mimicking the mechanical effects of internal growth processes. The increase of the internal pressure finally led to rupture of the cortical cylinders. The circumferential stresses acting on the inner surface of the cortical cylinders were calculated. These data allow quantitative estimates of the radial and circumferential pressures effected by vascular secondary growth processes during ontogeny in A. macrophylla stems. The experimental results further indicate that the outer sclerenchymatous cylinder is the main contributor to mechanical stability of young A. macrophylla stems.
Aristolochia macrophylla; biomechanics; ontogeny; primary organization; secondary growth; vine
A mathematical method, based on polar coordinates that allow modelling of primary and secondary growth processes in stems of extant and fossil plants, is summarized and its potential is discussed in comparison with numerical methods using digitizing tablets or electronic image analysing systems. As an example, the modelling of tissue distribution in the internode of an extant sphenopsid (Equisetum hyemale) is presented. In the second half of the paper we present new data of a functional analysis of stem structure and biomechanics of the early lignophyte Tetraxylopteris schmidtii (Middle Devonian) using the polar coordinate method for modelling the tissue distribution in stems of different ontogenetic age. Calculations of the mechanical properties of the stems, based on the modelling of the tissue arrangement, indicate that there is no increase in structural bending modulus throughout the entire development of the plant. The oldest ontogenetic stage has a significantly smaller bending elastic modulus than the intermediate ontogenetic stage, a 'mechanical signal', which is not consistent with a self-supporting growth form. These results, and the ontogenetic variations of the contributions of different stem tissues to the flexural stiffness of the entire stem, are discussed in the evolutionary context of cambial secondary growth.
Clematis flammula var. maritima is a woody lianoid plant that grows on coastal sand dunes in the Mediterranean region. Older perennial stems are present as extensive underground axes. These generate surface growth of shorter‐lived stems producing monospecific trellises above the surface of the sand. Despite its sand dune habitat and shortage of host support plants, this variety of Clematis shows mechanical characteristics during growth that are closely comparable with those of scandent woody lianas. A significant decrease in the value of structural Young’s modulus is observed from the aerial trellis‐forming shoots (1·619 ± 0·492 GN m–2) to emergent axes (0·855 ± 0·253 GN m–2) and underground woody stems (0·470 ± 0·113 GN m–2). Biomechanical and evelopmental observations indicate that most emergent branches are optimized geometrically and mechanically in relation to their points of emergence from the sand, with increases in structural Young’s modulus and the second moment of area around the surface of the sand. Lianoid plants, physiologically capable of withstanding sand dune environments, might represent acceptable natural or introduced species for dune stabilization and conservation.
Biomechanics; Clematis flammula var. maritima L.; growth habit; liana; sand dune