Sandrine Isnard

Moving with climbing plants from Charles Darwin’s time into the 21st century

We provide an overview of research on climbing plants from Charles Darwin to the present day. Following Darwins interests, this review will focus on functional perspectives including attachment mechanisms and stem structure and function. We draw attention to a number of unsolved problems inviting future research. These include the mechanism for establishment of the twining habit, a quantitative description following the development of a tissue element through space and time, the chemistry of sticky exudates, the microstructure of xylem and the capacity for water storage, the vulnerability to embolism, and the mechanism for embolism repair. In conclusion we cite evidence that, in response to increasing CO(2) concentration, anthropic perturbation and/ or increasing forest fragmentation, lianas are increasing relative to tree species. In the 21st century, we are returning to the multiscale, multidisciplinary approach taken by Darwin to understand natural history.

Diversity of Mechanical Architectures in Climbing Plants: An Evolutionary Perspective

Mechanical architectures of a wide range of climbing plants are reviewed from a wide phylogenetic range and evolutionary contingencies. They include an herbaceous lycopod (Lycopodiaceae) - a woody tropical liana (Apocynaceae), temperate climbers, herbs and shrubs (Ranunculacae), and two representative climbing palms (Arecoideae, Calamoideae). Trends in mechanical properties during development are reviewed and interpreted via changes in anatomical development of the stem and type of connection to host supports. The results indicate that there are some biomechanical features common to diverse climbing plants including (1) phases of relatively rigid stem growth where the climbing stem has to span between supports and (2) a mechanism to achieve greater compliancy towards the base or at points where the slender climbing stem is at risk from excessive mechanical stress. Evolutionary contingencies such as basal plesiomorphic constraint, complexification, simplification and developmental loss can drastically influence ways in which different plants have evolved different biomechanical climbing architectures. Two key developmental features controlling the biomechanics of the climbing stem are (1) the presence/absence of secondary growth and (2) the number, complexity and coordination of development of primary or secondary tissues with varying mechanical properties. Recent research has suggested that evolution of specialized climbing architectures can canalize subsequent evolution of alternative growth forms. The results suggest that the origin and type of climbing architecture can be heavily influenced by ancestral growth forms and architectures. Despite the extremely complex patterns of plant growth form evolution involving “escapes” to and from more specialized or simpler bauplans, selective pressure towards non-self-supporting growth forms is a remarkably persistent and iterative feature of growth form evolution in land plants.

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

UNLABELLED 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.

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.

Growth Form Evolution in Piperales and Its Relevance for Understanding Angiosperm Diversification: An Integrative Approach Combining Plant Architecture, Anatomy, and Biomechanics

A striking feature of early angiosperm lineages is the variety of life forms and growth forms, which ranges from herbs, aquatic herbs, climbers, and epiphytes to woody shrubs and trees. This morphological and anatomical diversity is arguably one of the factors explaining how angiosperms dominate many ecosystems worldwide. However, just how such a wide spectrum of growth forms has evolved in angiosperms remains unclear. In this review, we investigate patterns of growth form diversification in Piperales, an early-diverging lineage (with stem age estimated at 201–128 Myr ago) and the most morphologically diverse clade among magnoliids. We outline patterns of growth form diversity and architecture as well as the biomechanical significance of developmental characters, such the organization, loss, and gain of woodiness. Asaroideae and Saururaceae are terrestrial as well as semiaquatic to aquatic herbaceous perennials bearing rhizomes. The Aristolochioideae and Piperaceae show higher levels of growth form diversity and biomechanical organization, with complex patterns of increasing or decreasing woodiness and architectural organization. The climbing habit has probably evolved independently in the Aristolochiaceae and Piperaceae, while mechanically unstable shrubs and, less frequently, treelets have evolved several times within these two most species-rich clades. A key developmental character underlying diversity in most Piperales—with the exception of the herbaceous Saruma (Asaroideae)—is the conserved development of the wood cylinder, in which fusiform initials are limited to fascicular cambial initials. The resulting large fraction of raylike tissue in the stem—a highly characteristic feature of woody species in the Piperales—potentially introduced mechanical constraints on the diversification of self-supporting architectures. This was possibly circumvented by the architectural development of repeated, large-diameter meristems in some shrublike habits via sympodial growth. Patterns of growth form evolution within Piperales potentially mirror some of the overall trends observed among early-diverging angiosperms as a whole as well as angiosperms in general. These include profound changes in life form and growth form linked to large-scale transitions in woodiness, diversity of mechanical organization, and shifts in architectural development.

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.

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.

Biomechanics of climbing palms and how they climb

Climbing plants have fascinated botanists since the pioneering works of Darwin and his contemporaries in the 19th century. Diverse plants have evolved different ways of climbing and a wide range of attachment devices and stem biomechanics to cope with the particular physical demands of life as a climber. We investigated the biomechanics of attachment in a range of climbing palms, including true rattans from Southeast Asia and the genus Desmoncus from South America. We found that hook strength and orientation is coordinated with rachis geometry and rigidity. These findings support the notion of a ratchet-type attachment mechanism and partly explain why these spiny plants are so catchy and efficient at attaching to supports.

Stem biomechanics of the giant moss Dendroligotrichum dendroides s.l. and its significance for growth form diversity in mosses

Abstract The giant moss Dendroligotrichum dendroides s.l. grows as self-supporting plants up to 40 cm in height in forest habitats in Chile and New Zealand. This moss represents one of the tallest self-supporting bryophytes. Biomechanical tests indicate that the stems can develop a high degree of stiffness (Young’s modulus) via a dense hypodermal sterome that is comparable with that of woody stems of vascular plants. A comparison with mechanical properties of other terrestrial and aquatic mosses indicates that different moss growth and life forms can produce very different mechanical architectures. Values of stem stiffness can vary between different growth forms of mosses to a comparable extent to that observed among diverse growth forms of vascular plants. Plants varying profoundly in overall size, development, and phylogenetic position nevertheless appear to develop comparable mechanical adaptations and growth forms in response to certain environmental conditions.

Vulnerability to xylem embolism as a major correlate of the environmental distribution of rain forest species on a tropical island: Embolism vulnerability and rain forest species distribution

Increases in drought-induced tree mortality are being observed in tropical rain forests worldwide and are also likely to affect the geographical distribution of tropical vegetation. However, the mechanisms underlying the drought vulnerability and environmental distribution of tropical species have been little studied. We measured vulnerability to xylem embolism (P50 ) of 13 woody species endemic to New Caledonia and with different xylem conduit morphologies. We examined the relation between P50 , along with other leaf and xylem functional traits, and a range of habitat variables. Selected species had P50 values ranging between -4.03 and -2.00 MPa with most species falling in a narrow range of resistance to embolism above -2.7 MPa. Embolism vulnerability was significantly correlated with elevation, mean annual temperature and percentage of species occurrences located in rain forest habitats. Xylem conduit type did not explain variation in P50 . Commonly used functional traits such as wood density and leaf traits were not related to embolism vulnerability. Xylem embolism vulnerability stands out among other commonly used functional traits as a major driver of species environmental distribution. Drought-induced xylem embolism vulnerability behaves as a physiological trait closely associated with the habitat occupation of rain forest woody species.