A 2D model to study how secondary growth affects the self-supporting behaviour of climbing plants.

Climbing plants exhibit specialized shoots, called "searchers", to cross spaces and alternate between spatially discontinuous supports in their natural habitats. To achieve this task, searcher shoots combine both primary and secondary growth processes of their stems in order to support, orientate and explore their extensional growth into the environment. Currently, there is an increasing interest in developing models to describe plant growth and posture. However, the interactions between the sensing activity (e.g. photo-, gravi-, proprioceptive sensing) and the elastic responses are not yet fully understood. Here, we aim to model the extension and rigidification of searcher shoots. Our model defines variations in the radius (and consequently in mass distribution) along the shoot based on experimental data collected in natural habitats of two climbing species: Trachelospermum jasminoides (Lindl.) Lem. and Condylocarpon guianense Desf.. Using this framework, we predicted the sensory aspect of a plant, that is, the plant's response to external stimuli, and the plant's proprioception, that is, the plant's "self-awareness". The results suggest that the inclusion of the secondary growth in a model is fundamental to predict the postural development and self-supporting growth phase of shoots in climbing plants.

Failure without Tears: Two-Step Attachment in a Climbing Cactus.

Climbing plants can be extremely adaptable to diverse habitats and capable of colonising perturbed, unstructured, and even moving environments. The timing of the attachment process, whether instantaneous (e.g., a pre-formed hook) or slow (growth process), crucially depends on the environmental context and the evolutionary history of the group concerned. We observed how spines and adhesive roots develop and tested their mechanical strength in the climbing cactus Selenicereus setaceus (Cactaceae) in its natural habitat. Spines are formed on the edges of the triangular cross-section of the climbing stem and originate in soft axillary buds (areoles). Roots are formed in the inner hard core of the stem (wood cylinder) and grow via tunnelling through soft tissue, emerging from the outer skin. We measured maximal spine strength and root strength via simple tensile tests using a field measuring Instron device. Spine and root strengths differ, and this has a biological significance for the support of the stem. Our measurements indicate that the measured mean strength of a single spine could theoretically support an average force of 2.8 N. This corresponds to an equivalent stem length of 2.62 m (mass of 285 g). The measured mean strength of root could theoretically support an average of 13.71 N. This corresponds to a stem length of 12.91 m (mass of 1398 g). We introduce the notion of two-step attachment in climbing plants. In this cactus, the first step deploys hooks that attach to a substrate; this process is instantaneous and is highly adapted for moving environments. The second step involves more solid root attachment to the substrate involving slower growth processes. We discuss how initial fast hook attachment can steady the plant on supports allowing for the slower root attachment. This is likely to be important in wind-prone and moving environmental conditions. We also explore how two-step anchoring mechanisms are of interest for technical applications, particularly for soft-bodied artefacts, which must safely deploy hard and stiff materials originating from a soft compliant body.

Microspines in tropical climbing plants: a small-scale fix for life in an obstacle course.

Many climbing plants have microspines on their stems, which facilitate attachment and prevent slipping and falling from host plant supports. Extending via growth through complex environments and anchoring stems to substrates with minimal contact forces are key benefits for climbing plants. Microspines are also highly desirable features for new technologies and applications in soft robotics. Using a novel sled-like device, we investigated static and sliding attachment forces generated by stems in 10 species of tropical climber from French Guiana differing in size and climbing habit. Eight species showed higher static and sliding forces when their stems were pulled in the basal direction against a standard surface than in the apical direction. This anisotropic behaviour suggests that tropical climbers have evolved different ratchet-like mechanisms that allow easy sliding forwards but are resistant to slipping downwards. The presence of a downwards 'stick-and-slip' phenomenon, where static attachment is not significantly stronger than maximal sliding attachment, was present in most species apart from three showing relatively weak attachment by microspines. This indicates that diverse microspine attachment strategies exist in climbing plants. This diversity of functional properties offers a range of potential design specifications for climbing strategies on different substrates for artificial climbing artefacts.

Trellis-forming stems of a tropical liana Condylocarpon guianense (Apocynaceae): A plant-made safety net constructed by simple "start-stop" development.

Tropical vines and lianas have evolved mechanisms to avoid mechanical damage during their climbing life histories. We explore the mechanical properties and stem development of a tropical climber that develops trellises in tropical rain forest canopies. We measured the young stems of Condylocarpon guianensis (Apocynaceae) that construct complex trellises via self-supporting shoots, attached stems, and unattached pendulous stems. The results suggest that, in this species, there is a size (stem diameter) and developmental threshold at which plant shoots will make the developmental transition from stiff young shoots to later flexible stem properties. Shoots that do not find a support remain stiff, becoming pendulous and retaining numerous leaves. The formation of a second TYPE II (lianoid) wood is triggered by attachment, guaranteeing increased flexibility of light-structured shoots that transition from self-supporting searchers to inter-connected net-like trellis components. The results suggest that this species shows a "hard-wired" development that limits self-supporting growth among the slender stems that make up a liana trellis. The strategy is linked to a stem-twining climbing mode and promotes a rapid transition to flexible trellis elements in cluttered densely branched tropical forest habitats. These are situations that are prone to mechanical perturbation via wind action, tree falls, and branch movements. The findings suggest that some twining lianas are mechanically fine-tuned to produce trellises in specific habitats. Trellis building is carried out by young shoots that can perform very different functions via subtle development changes to ensure a safe space occupation of the liana canopy.

Structural performance of a climbing cactus: making the most of softness.

Climbing plants must reach supports and navigate gaps to colonize trees. This requires a structural organization ensuring the rigidity of so-called 'searcher' stems. Cacti have succulent stems adapted for water storage in dry habitats. We investigate how a climbing cactus Selenicereus setaceus develops its stem structure and succulent tissues for climbing. We applied a 'wide scale' approach combining field-based bending, tensile and swellability tests with fine-scale rheological, compression and anatomical analyses in laboratory conditions. Gap-spanning 'searcher' stems rely significantly on the soft cortex and outer skin of the stem for rigidity in bending (60-94%). A woody core contributes significantly to axial and radial compressive strength (80%). Rheological tests indicated that storage moduli were consistently higher than loss moduli indicating that the mucilaginous cortical tissue behaved like a viscoelastic solid with properties similar to physical or chemical hydrogels. Rheological and compression properties of the soft tissue changed from young to old stages. The hydrogel-skin composite is a multi-functional structure contributing to rigidity in searcher stems but also imparting compliance and benign failure in environmental situations when stems must fail. Soft tissue composites changing in function via changes in development and turgescence have a great potential for exploring candidate materials for technical applications.

Mechanical Innovations of a Climbing Cactus: Functional Insights for a New Generation of Growing Robots.

Climbing plants are being increasingly viewed as models for bioinspired growing robots capable of spanning voids and attaching to diverse substrates. We explore the functional traits of the climbing cactus Selenicereus setaceus (Cactaceae) from the Atlantic forest of Brazil and discuss the potential of these traits for robotics applications. The plant is capable of growing through highly unstructured habitats and attaching to variable substrates including soil, leaf litter, tree surfaces, rocks, and fine branches of tree canopies in wind-blown conditions. Stems develop highly variable cross-sectional geometries at different stages of growth. They include cylindrical basal stems, triangular climbing stems and apical star-shaped stems searching for supports. Searcher stems develop relatively rigid properties for a given cross-sectional area and are capable of spanning voids of up to 1 m. Optimization of rigidity in searcher stems provide some potential design ideas for additive engineering technologies where climbing robotic artifacts must limit materials and mass for curbing bending moments and buckling while climbing and searching. A two-step attachment mechanism involves deployment of recurved, multi-angled spines that grapple on to wide ranging surfaces holding the stem in place for more solid attachment via root growth from the stem. The cactus is an instructive example of how light mass searchers with a winged profile and two step attachment strategies can facilitate traversing voids and making reliable attachment to a wide range of supports and surfaces.

Bouldering: an alternative strategy to long-vertical climbing in root-climbing hortensias.

In the Neotropics, the genus Hydrangea of the popular ornamental hortensia family is represented by climbing species that strongly cling to their support surface by means of adhesive roots closely positioned along specialized anchoring stems. These root-climbing hortensia species belong to the nearly exclusive American Hydrangea section Cornidia and generally are long lianescent climbers that mostly flower and fructify high in the host tree canopy. The Mexican species Hydrangea seemannii, however, encompasses not only long lianescent climbers of large vertical rock walls and coniferous trees, but also short 'shrub-like' climbers on small rounded boulders. To investigate growth form plasticity in root-climbing hortensia species, we tested the hypothesis that support variability (e.g. differences in size and shape) promotes plastic responses observable at the mechanical, structural and anatomical level. Stem bending properties, architectural axis categorization, tissue organization and wood density were compared between boulder and long-vertical tree-climbers of H. seemannii. For comparison, the mechanical patterns of a closely related, strictly long-vertical tree-climbing species were investigated. Hydrangea seemannii has fine-tuned morphological, mechanical and anatomical responses to support variability suggesting the presence of two alternative root-climbing strategies that are optimized for their particular environmental conditions. Our results suggest that variation of some stem anatomical traits provides a buffering effect that regulates the mechanical and hydraulic demands of two distinct plant architectures. The adaptive value of observed plastic responses and the importance of considering growth form plasticity in evolutionary and conservation studies are discussed.

Major trends in stem anatomy and growth forms in the perianth-bearing Piperales, with special focus on Aristolochia.

BACKGROUND AND AIMS: The order Piperales has the highest diversity of growth forms among the earliest angiosperm lineages, including trees, shrubs, climbers and herbs. However, within the perianth-bearing Piperales (Asarum, Saruma, Lactoris, Hydnora, Prosopanche, Thottea and Aristolochia), climbing species only occur in the most species-rich genus Aristolochia. This study traces anatomical and morphological traits among these lineages, to detect trends in growth form evolution and developmental processes. METHODS: Transverse stem sections of different developmental stages of representatives of Asarum, Saruma, Lactoris, Hydnora, Thottea and Aristolochia were compared and anatomical traits were linked to growth form evolution. Biomechanical properties of representative climbers were determined in three-point bending tests and are discussed based on the anatomical observations. Growth form evolution of the perianth-bearing Piperales was reconstructed by ancestral character state reconstruction using Mesquite. KEY RESULTS: While species of Asarum and Saruma are exclusively herbaceous, species of the remaining genera show a higher diversity of growth habit and anatomy. This growth form diversity is accompanied by a more complex stem anatomy and appropriate biomechanical properties. The ancestral growth form of the perianth-bearing Piperales is reconstructed with either a shrub-like or herbaceous character state, while the following three backbone nodes in the reconstruction show a shrub-like character state. Accordingly, the climbing habit most probably evolved in the ancestor of Aristolochia. CONCLUSIONS: Since the ancestor of the perianth-bearing Piperales has been reconstructed with a herb- or shrub-like habit, it is proposed that the climbing habit is a derived growth form, which evolved with the diversification of Aristolochia, and might have been a key feature for its diversification. Observed anatomical synapomorphies, such as the perivascular fibres in Lactoris, Thottea and Aristolochia, support the phylogenetic relationship of several lineages within the perianth-bearing Piperales. In addition, the hypothesis that the vegetative organs of the holoparasitic Hydnoraceae are most probably rhizomes is confirmed.

Global diversification of a tropical plant growth form: environmental correlates and historical contingencies in climbing palms.

Tropical rain forests (TRF) are the most diverse terrestrial biome on Earth, but the diversification dynamics of their constituent growth forms remain largely unexplored. Climbing plants contribute significantly to species diversity and ecosystem processes in TRF. We investigate the broad-scale patterns and drivers of species richness as well as the diversification history of climbing and non-climbing palms (Arecaceae). We quantify to what extent macroecological diversity patterns are related to contemporary climate, forest canopy height, and paleoclimatic changes. We test whether diversification rates are higher for climbing than non-climbing palms and estimate the origin of the climbing habit. Climbers account for 22% of global palm species diversity, mostly concentrated in Southeast Asia. Global variation in climbing palm species richness can be partly explained by past and present-day climate and rain forest canopy height, but regional differences in residual species richness after accounting for current and past differences in environment suggest a strong role of historical contingencies in climbing palm diversification. Climbing palms show a higher net diversification rate than non-climbers. Diversification analyses of palms detected a diversification rate increase along the branches leading to the most species-rich clade of climbers. Ancestral character reconstructions revealed that the climbing habit originated between early Eocene and Miocene. These results imply that changes from non-climbing to climbing habits may have played an important role in palm diversification, resulting in the origin of one fifth of all palm species. We suggest that, in addition to current climate and paleoclimatic changes after the late Neogene, present-day diversity of climbing palms can be explained by morpho-anatomical innovations, the biogeographic history of Southeast Asia, and/or ecological opportunities due to the diversification of high-stature dipterocarps in Asian TRFs.

The evolutionary fate of phenotypic plasticity and functional traits under domestication in manioc: changes in stem biomechanics and the appearance of stem brittleness.

Domestication can influence many functional traits in plants, from overall life-history and growth form to wood density and cell wall ultrastructure. Such changes can increase fitness of the domesticate in agricultural environments but may negatively affect survival in the wild. We studied effects of domestication on stem biomechanics in manioc by comparing domesticated and ancestral wild taxa from two different regions of greater Amazonia. We compared mechanical properties, tissue organisation and wood characteristics including microfibril angles in both wild and domesticated plants, each growing in two different habitats (forest or savannah) and varying in growth form (shrub or liana). Wild taxa grew as shrubs in open savannah but as lianas in overgrown and forested habitats. Growth form plasticity was retained in domesticated manioc. However, stems of the domesticate showed brittle failure. Wild plants differed in mechanical architecture between shrub and liana phenotypes, a difference that diminished between shrubs and lianas of the domesticate. Stems of wild plants were generally stiffer, failed at higher bending stresses and were less prone to brittle fracture compared with shrub and liana phenotypes of the domesticate. Biomechanical differences between stems of wild and domesticated plants were mainly due to changes in wood density and cellulose microfibril angle rather than changes in secondary growth or tissue geometry. Domestication did not significantly modify "large-scale" trait development or growth form plasticity, since both wild and domesticated manioc can develop as shrubs or lianas. However, "finer-scale" developmental traits crucial to mechanical stability and thus ecological success of the plant were significantly modified. This profoundly influenced the likelihood of brittle failure, particularly in long climbing stems, thereby also influencing the survival of the domesticate in natural situations vulnerable to mechanical perturbation. We discuss the different selective pressures that could explain evolutionary modifications of stem biomechanical properties under domestication in manioc.

Escaping the lianoid habit: evolution of shrub-like growth forms in Aristolochia subgenus Isotrema (Aristolochiaceae).

PREMISE OF THE STUDY: A large range of growth forms is a notable aspect of angiosperm diversity and arguably a key element of their success. However, few studies within a phylogenetic context have explored how anatomical, developmental, and biomechanical traits are linked with growth form evolution. Aristolochia (∼500 species) consists predominantly of climbers, but a handful of shrub-like species are known from Aristolochia subgenus Isotrema (hereafter, shortened to Isotrema). We test hypotheses proposing that the establishment of functional traits linked to lianescence might limit the ability to evolve structurally diverse growth forms, particularly self-supporting forms. • METHODS: We focus on the origin of the shrub habit in Isotrema, from which we sampled representatives from climbing to self-supporting forms. Morphological, anatomical, and biomechanical characters are optimized on a chloroplast- and nuclear-derived phylogeny. • KEY RESULTS: Character-state reconstructions revealed that the climbing habit is plesiomorphic in Isotrema and shrub-like forms are derived from climbers. However, shrubs do not constitute a monophyletic group. Both shrubs and climbers show large multiseriate rays, but differ in terms of vessel size and proportion of fibers and soft tissues. • CONCLUSION: We suggest that while shrub-like species might have partly escaped from the constraints of life as lianas; their height size and stability are not typical of self-supporting shrubs and trees. Shrubs retained lianoid stem characters that are known to promote flexibility such as ray parenchyma. The transitions to a shrub-like form likely involved relatively simple, developmental changes that may be attributed to heterochronic processes.

The climbing habit in palms: Biomechanics of the cirrus and flagellum.

Climbing palms in the Arecoideae (Desmoncus) and Calamoideae (rattan palms) both evolved cirrate leaves armed with hooks and grapnels for climbing. Some species of Calamoideae develop a different climbing organ known as the flagellum, which also bears hooks. The present study indicates that geometry and mechanical properties of the cirrus vary between species. Cirrate leaves are constructed to optimize bending and torsion in relation to the deployment of recurved hooks. Hook development, size, and strength vary along cirri and flagella and are consistent with observations of these attachment organs functioning as a ratchet mechanism: hooks increase in strength toward the base of attachment organs and always fail before the axis in strength tests. Hook size and strength differ between species and are related to body size and ecological preference. Larger species produce larger hooks, but smaller climbing palms of the understory deploy fine sharp hooks that are effective on small diameter supports as well as large branches and trunks. The ephemeral nature of climbing organs in palms provides a challenge to their life-history development, particularly in terms of mechanical constraints and remaining attached to the host vegetation; these differ significantly from many vines and lianas having more perennial modes of attachment.

Evolution of shrub-like growth forms in the lianoid subfamily Secamonoideae (Apocynaceae s.l.) of Madagascar: phylogeny, biomechanics, and development.

Lianas are common in the Apocynaceae s.l. and are predominant in the subfamily Secamonoideae. Shrub-like taxa are rare within this subfamily but occur in Malagasy genera such as Secamone, Secamonopsis, and Pervillaea. We explored the evolutionary appearance of shrub-like growth forms in Malagasy Secamonoideae through a molecular phylogeny using chloroplastic sequences. The phylogeny revealed several independent appearances of shrub-like growth forms within the Secamonoideae. Biomechanics and development of the shrub-like growth form were detailed in one species, Secamone sparsiflora, which has upright and self-supporting young stems that become procumbent in older stages of development. Biomechanical investigations revealed characteristics atypical of both lianas and self-supporting shrubs. Anatomical development in S. sparsiflora is initially similar to lianas in the same clade but shows potentially neotenic retention of juvenile wood development for most of the growth trajectory. The results suggest that evolution of lianescence can carry a high degree of specialization and developmental burden that might limit evolution back to self-supporting growth forms. Under certain geographic and ecological conditions, such as geographic isolation, xeric conditions and/or reduced biotic competition, escapes from lianescence to other growth forms can occur in some angiosperm groups via relatively simple heterochronic shifts of mechanically significant growth processes.

Biomechanics and development of the climbing habit in two species of the South American palm genus Desmoncus (Arecaceae).

Mechanical properties are investigated in Desmoncus orthacanthos and D. polyacanthos from French Guiana, South America. Differences in size and axis stiffness are related to different trellis requirements and habitats. The leaf sheath surrounds the stem, increasing stiffness of young self-supporting stages and apical parts of older climbing plants. Senescence of the leaf sheath reduces stiffness of older climbing axes of both species. Its eventual loss in D. orthacanthos facilitates deformation into coils and loops when plants slip from their supports following senescence of leaves bearing attachment organs. In smaller climbing axes of D. polyacanthos, the senescent leaf sheath remains attached and axes rarely form loops and coils below attachment. An increase in stiff mechanical properties toward the base of both species is radically different from that of many dicotyledonous lianas. Besides the presence of attachment organs, stem mechanical properties of Desmoncus are similar to those of erect though not fully self-supporting stems of Bactris major, a sympatric species of the sister group genus to Desmoncus. The climbing habit in Desmoncus may have evolved via (1) heterochronic processes including early elongation of internodes relative to increase in stem diameter (reduction of the establishment phase) and (2) increased persistence of leaf sheaths.

Modelling primary and secondary growth processes in plants: a summary of the methodology and new data from an early lignophyte.

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.