How Vines Climb: Still Working On Figuring That Out

Twining plants

The graceful movements of twining plants—revolving in large arcs, winding around a support, and forming a helical tube of tissue—have fascinated biologists since the 19th century (Darwin, 1865, 1880; Sachs, 1874; Baillaud, 1968). Particularly, authors noted the revolving movement that occurs in the two or three internodes below the apical bud (see video in Appendix S1 in Supplemental Data with the online version of this article). Darwin described this movement as “a continuous self-bowing of the whole shoot, successively directed to all points of the compass” (Darwin, 1865, p.7) and later named this movement circumnutation (Darwin, 1880, p.1). Circumnutation is a common phenomenon in plants but is exaggerated in twining stems. By circumnutating, twiners increase the probability of encountering a support. Young twining plants exhibit exploratory movements, circumnutating with large radius (reviewed in Baillaud, 1968). The form of the shoot is straight and vertical at the base, straight and horizontal near the apex, and curved in a plane in what seems to be the business part of the circumnutating stem. When the stem encounters a vertical support, the habit and the rhythmic pattern change. The period of revolution increases from approximately 2 to more than 9 h (Darwin, 1865; Baillaud, 1968). The stem executes a complex dance, moving rhythmically as it appears to undulate upward around its supporting pole (see video in Appendix S2 in online Supplemental Data). A coil surrounds the pole, soon tightening basally into a helix that wraps snugly around the pole and leaves a corkscrew-shaped stem.

The primary growth zone of twining stems is long, extending 12 or even 20 cm from the apex through the bending zone and into the first helical gyre (Silk and Abou Haidar, 1986; Isnard et al., 2009). Once a stem is coiled around a support, it generally shows an antidromous twist, i.e., a twist of the stem around its own axis opposing the direction of the revolving movement. Darwin observed that the stem twist (angle of twist per unit length of stem) increased with the roughness of the surface texture of the support. However, these observations have not been extended or quantified. It is clear that a twining plant forms a helical tube of twisted tissue as it grows around a vertical stem or other cylindrical support (Fig. 2). The mature stem twining on a support of uniform diameter has uniform curvature and torsion (alternatively, uniform radius and wavelength). The handedness of the helix is mostly genetically determined. The majority of species make right-handed helices (viewed from above they wind counter-clockwise around their supports), but a substantial minority of species (including Dioscorea spp., Dioscoreaceae; and Humulusspp., Cannabaceae) are left-handed (Darwin, 1865; Baillaud, 1968). The stem geometry has been found to change in a predictable way with the diameter of the supporting structure (Bell, 1958; Putz and Holbrook, 1991). On thicker supports, the vine makes coils with longer wavelengths and smaller curvature and torsion.

When the stem reaches the top of a supporting pole, it actually unwinds its apical gyre and resumes the large circumnutation of the searching habit. Also, if the support is inclined away from the vertical, the vine unwraps and resumes the exploratory movements. Darwin observed that in some species if the stem does not encounter a vertical support, it grows downward and then twines upward around the older part of the existing shoot (Darwin, 1865).

The underlying mechanism of circumnutation has long remained obscure. Darwin (1865, p. 19) first proposed that circumnutation depend on “the contraction or turgescence of the cells circulating round the axis.” In his later book (Darwin, 1875, p.32), he proposed that circumnutation will depend on “the rate at which growth travels or circulates round the axis.” This last hypothesis suggests that an endogenous oscillator produces a growth wave traveling around the elongating stem. The underlying mechanism of this “endogenous oscillator,” however, still remains obscure. For a long time, the curvature of a circumnutating stem was thought to be the consequence of unequal growth on the opposite sides of the shoot (Darwin, 1875; Baillaud, 1968). Millet et al. (1988), however, showed that circumnutation of Phaseolus vulgaris (Fabaceae) twining shoot cannot be explained solely by growth. They found that oscillations in the revolving movement were correlated with periodic, partly reversible, turgor-mediated volume changes in the epidermal cells of the bending zone (Caré et al., 1998). Thus, circumnutation appears to involve periodic, reversible cell volume changes superimposed on a regular, irreversible expansion pattern.

There is by now data on the generation of traveling waves of solute, water, and other growth-inducing substances (Millet et al., 1988; Lubkin, 1994). There are also time-lapse growth records showing circumnutating and twining stems with associated spatial and temporal oscillations in stem curvature and torsion. However, a comprehensive analysis of the growth rate pattern producing the morphogenesis is lacking. In particular, no one has tabulated the geometry changes associated with the growth of a tissue element during its displacement from the apex through the revolving and twining zones. A subtle point is assessment of the relative importance of local and convective curvature changes. The need for this approach is evident in an analysis of growth rate patterns that produce a hypocotyl curvature (Fig. 3). Surface marks flow through the hook during its growth; thus, we realize that the curved form of the hypocotyl hook is maintained by a parade of tissue elements, each of which first curves and then straightens. Therefore, to produce the hook, the stem grows faster on the convex side near the apex (where curvature is increasing) and on the concave side near the base of the hook (where curvature is decreasing). During hook maintenance (under soil and in dim light), convective curvature change, that is, the change associated with movement to a region with different curvature, is dominant; “local” change is negligible. In bright light, the hook straightens. During the straightening process, the inside of the hook grows, while the outside stops growing and even shrinks for a time. Convective curvature change is negligible; the straightening process is dominated by local changes. This two-dimensional problem suggests that a growth analysis of a twining vine, following expansion and rotation of material tissue elements through space and time needs to be coupled to physiological studies provided earlier for water relations, wall mechanics, hormone involvement, and ion fluxes.

The Shidare-asagao mutant of morning glory (Ipomoea nil, Fabaceae) (weeping habit) fails to twine and also lacks shoot gravitropism (Hatakeda et al., 2003;Kitazawa et al., 2005; Kiss, 2006). Molecular and structural studies led to the exciting discovery that a modified SCR gene appears to be responsible for both an abnormality in gravisensing endodermal cells and the loss of circumnutation and twining (Hatakeda et al., 2003; Kitazawa et al., 2005; Kiss, 2006). This result, although providing clear evidence that SCR is necessary for gravisensing and twining, does not show that gravisensing is in general necessary for circumnutation. Earlier spaceflight experiments showed that circumnutations in sunflower hypocotyls occur in the absence of gravity (Brown, 1993). However, the reduction of period and amplitude of circumnutation in space flight indicates that gravity does play a modifying role (Brown, 1993). In the absence of gravity, the stem would not achieve appropriate revolving movements, which are necessary for the plant to twine around supports.

Recent work on the twining habit has focused on the biomechanical aspects of the twining habit, particularly how twiners avoid slipping down their support. A central notion is that the twining stem might generate a squeezing force or normal load directed toward the support to maintain its position (Silk, 1989a,1989b). Silk and Hubbard (1991) first measured the squeezing force of a twiner by wrapping a stem of Pharbitis nil (syn. Ipomoea acuminata, Convolvulaceae) around a water-filled balloon of the same diameter as its support. They also showed that when the vine was removed from its support, it would tend to twist up, reducing the radius, the wavelength, and the arc length of the helix while simultaneously increasing its torsion. Measurements of squeezing force in situ were done later using an electronic device made up of a split pole where the plant, while twining, acts to pull the halves of the pole together, causing deformation of load cells (Matista and Silk, 1997). Inward forces and the importance of frictional interactions in maintaining the stability of the twining habit have thus been emphasized using this device (Matista and Silk, 1997; Silk et al., 2000; Silk and Holbrook, 2005). These studies confirm the idea that the stem of a twining vine uses a helical geometry to generate a normal load directed toward the support, but they failed to explain how vines generate such force during growth. Hydrostatic inflation was proposed to produce contact forces with the pole (Silk and Hubbard, 1991), but Silk et al. (2000) later showed that 50–90% of the twining force remained after dehydration inPharbitis nil and Dioscorea bulbifera, suggesting that forces other than turgor pressure must be involved in maintaining the twining habit. Scher et al. (2001)could not find a consistent relationship between the timing of fiber maturation and the generation of squeezing force. Secondary growth may of course contribute to the tightening of the helical form by reducing the inner diameter of the helix, but some twiners are monocotyledons lacking secondary growth. Furthermore, a significant fraction of the twining force has been shown to develop during the formation of the first gyre, while stem diameter did not change (Scher et al., 2001).

Recently Isnard et al. (2009) proposed a solution to the riddle of the helical squeezing force when they discovered that a modest radial stem expansion during primary growth or the growth of lateral structures such as leaf bases can significantly contribute to the squeezing force by putting the helical stem under tension. The authors built an improved force-sensing device to measure squeezing forces in the monocot Dioscorea bulbifera, and they used time-lapse photography to document the trajectory of the apex and the development of the helical form on the pole concomitant with monitoring of the squeezing force. Stipules developing on both side of the petiole base were observed to form discontinuous points of contact between the stem and its support. Experimental data and a simple thin rod model showed that growth of these stipules push the stem away from the support, effectively placing the stem in tension and generating a normal force on the pole (Isnard et al., 2009). In the earliest literature, Sachs (1874) noted that the petioles of some twining vine may be pinched between the stem and the support. However, the significance of this type of structure has long been overlooked, and these new results implied that any kind of pulvinus, stipule, or petiole base that is trapped between the stem and its support could be an effective mechanism for generating squeezing forces in twining plant. A survey of twining species morphologies reveals that this kind of structure is actually common among monocot and dicot twiners (e.g., the stipule in Humulus lupulus, the curved petiole base in some species of Dioscorea and in the twining bean Phaseolus vulgaris, the pulvinate petiole in twining Menispermaceae).

The helical form causes the twining vine to be very unstable in compression but extraordinarily stable in tension, preventing slipping under gravitational loads (Silk and Holbrook, 2005) (Fig. 4). The stability of twining vines under gravitational loads suggests an important role for friction. The coefficient of friction between vine stems and wood is high, often five times greater than between leather and wood, as determined by slip tests on an inclined plane. A mathematical model predicts that the stability of the vine in tension increases exponentially with the product of the coefficient of friction, the stem curvature, and the length of the twining stem. Thus, large masses (up to hundreds of kilograms) must be applied to the base of a twining vine to cause slipping (Silk and Holbrook, 2005). In contrast, twining vines are unstable in compression, collapsing when small masses (<10 g) are hung from the top of the vine (Fig. 4). However, if the loads are applied below the uppermost gyre, the stabilizing tensional effect dominates. Therefore, in nature vines twining on a cylindrical support are stable under gravitational loads, unless these loads occur near the apex. A corollary is that a short apical coil can hold up large masses of maturing shoot. Observations of Dioscorea bulbifera (Isnard et al., 2009) confirmed that the apical last gyre can support a substantial portion of manually uncoiled twining stems (7–10 gyres). The early establishment of the helical form can be aided by hooked trichomes in Humulus lupulus (Fig. 5) or stiff, reflexed hair in Doliocarpus major (Putz, 1984). In Ipomoea purpurea, stem trichomes function like ratchets to facilitate climbing upward (Silk and Holbrook, 2005).

Another interesting discovery is the widespread occurrence of gelatinous contractile fibers in the coiled regions of tendrils and twining stems (Meloche et al., 2007; Bowling and Vaughn, 2008, 2009). The placement of these fibers within tendril and stem cross-sections is suggestive of a role in twining (and tendril coiling, discussed later). The gelatinous fibers in twining plants appear to develop after primary growth has ceased so they probably contribute to the augmentation rather than the establishment of the twining force. It would be instructive to see whether increases in G-fibers parallel the increases in stem twisting that Darwin saw when stems twine on rough surfaces.

All the mechanisms described can explain only the generation of the squeezing force after the establishment of a gyre on the pole. Despite recent advances in the understanding of the biomechanics of twining plant, the mechanism by which the apical gyre grips the support remains unclear. Using energy considerations, Isnard et al. (2009) have shown that stem twist is important in producing the initial twining force exerted by the vine on its support. Further studies should focus on the mechanical attributes, the motion of the turgescent apical shoot, the early formation of the apical gyre on a cylindrical pole, and the mechanism of stem twist during growth.

Leaf-climbers and irritable organs

Darwin included in this type of attachment what he called leaf-bearers (e.g.,Clematis, Ranunculaceae), climbing by the aid of a sensitive petiole that bends and clasps the support after contact (Fig. 6A). He noted that they become woody and sometimes develop an internal structure like that of the stem (Fig. 6C). Leaf-climbers circumnutate more rapidly than twining plants and are distinguished also by their “irritability” (sensitivity to touch). We also include in this section sensitive organs or hooks, which resemble leaf-bearers in that they thicken while contacting a support. Treub (1883) and Ewart (1898) extensively studied this type of attachment in many tropical lianas. Such irritable organs include modified branches (Strychnos, Loganiaceae) or peduncles (Uncaria, Rubiaceae; Artabotrys, Annonaceae), which express irritability exclusively through a thickening in response to pressure or friction (Treub, 1883). Hook thickening may depend on cambial activity (Treub, 1883; Ewart, 1898). Rowe et al. (2006) noted that hooks in Strychnos sp. thicken and eventually close around supports. In the genus Uncaria, Treub (1883) noted that the wood in thickened hooks only contains tracheids and parenchyma, lacking vessels.Ewart (1898) found that larger hooks in Uncaria support a weight of 15 kg before breaking; hooks always broke at the point of attachment to the parent stem. He concluded that such a firmly attached hook can support a great length of stem. Free hooks that do not thicken are less robust than attached ones (Ewart, 1898) (Fig. 6B). Interestingly, Ewart noted a relation between the strength of fully developed hooks and the weight of a given length of stem. The maximum stem length a hook can support was remarkably similar among hook species.

Tendril-bearers

“It first places its tendrils ready for action, as a polypus places its tentacula.—”Darwin (1865, p. 118)

Tendrils are long, slender, filiform, irritable organs, derived from stems, leaves, or flower peduncles (Darwin, 1865) (Fig. 6D). They may occur either as unbranched or multibranched organs. Their length may vary from 3.8 cm inBignonia unguis (Bignoniaceae) to 40 cm in Vitis vinifera (Vitaceae) (Jaffe and Galston, 1968). Tendril-bearers circumnutate like twining plants, but differ from the latter in their faster and irregular ellipsoidal movements and their irritability. Tendril-bearers also differ from twining plants in that the direction of circumnutation is variable even in the same individual (Darwin, 1865). Older physiological studies of tendrils are reviewed by Jaffe and Galston (1968) and by Putz and Holbrook (1991). Jaffe and Galston described three main movements of tendrils: (1) circumnutation, an endogenous movement increasing the probability of contact with supports; (2) contact coiling, in which the stimulated tendril coils around a support, and (3) free coiling, in which the tendril develops helical coils along its axis, not necessarily as a result of stimulation. The contact coiling involves perception of a mechanical stimulus resulting in a complex chain of events, including fast ionic processes as well as chemical signaling to coordinate the reactions of the whole organ (Liss and Weiler, 1994; Engelberth et al., 1995). The subsequent free coiling of the tendril draws the stem closer to the support (Macdougal, 1896; Putz and Holbrook, 1991) and “provides the plant with an elastic spring-like connection to the support that enables it to resist high winds and loads” (McMillen and Goriely, 2002, p. 243). This free coiling leads to two helical structures with opposite handedness (Fig. 6D) (Darwin, 1865; Jaffe and Galston, 1968). As observed by Darwin (1865, p. 97), “When a tendril has caught a support and has spirally contracted, there are always as many turns in one direction as in the other; so that the twisting of the axis in the one direction is exactly compensated by that in the other.” Inversion of handedness, known as perversion, appears in a wide range of biological and physical systems and has been investigated for tendrils by Goriely and colleagues using the physics of thin elastic rods (Goriely and Tabor, 1998; McMillen and Goriely, 2002). “In order to create a helix during the free coiling, one of the ends must rotate. Since neither the stem nor the support can rotate, the total twist in the tendril cannot change. The solution will be to form two helices together with a small inversion” (McMillen and Goriely, 2002, p. 243).

An anatomical mechanism, involving gelatinous fibers, by which a tendril can squeeze a support has been recently proposed for redvine (Brunnichia ovata, Polygonaceae) and other species (Meloche et al., 2007; Bowling and Vaughn, 2009). Contracting gelatinous fibers are generally found in reaction wood where they are known to generate tensile growth stress and produce bending of branches (Yoshida et al., 2002; Pilate et al., 2004; Yamamoto, 2004). Interestingly, the distribution of gelatinous fibers in the tendril has been shown to vary with the type of tendril (Bowling and Vaughn, 2009). Tendrils coiling in all directions have gelatinous fibers distributed in a hollow cylinder at the periphery of the stem, while in tendril coiling in only one direction gelatinous fibers appear only on the concave side. Because these fibers occur when tendrils convert from straight to coiled structures, they concluded that gelatinous fibers contribute to the coiling and eventually to fixation and secure anchorage of the vine to the support.

Clinging climbers

We include in this type of climbers both root-climbers (e.g., Hedera helix) and adhesive tendril-climbers (e.g., Parthenocissus tricuspidata), that attach to tree trunks with glandular secretions or by growing into irregularities in the host bark (Fig. 7A, C). This mode of attachment allows climbers to ascend supports of almost any diameter or texture (Darwin, 1865; Putz, 1984; Hegarty, 1991;Groot et al., 2003). However, it is unusual for this type of climber to extend to more than a primary host tree because the mode of attachment requires close contact with a surface to adhere.

Darwin (1865) was struck by the properties of “viscid fluid” produced by rootlets of Ficus repens. He conducted a simple experiment, spreading a drop of the fluid on a glass plate with some grains of sand. He left the glass exposed in a drawer during hot and dry weather and found that after 128 d the fluid still surrounded each grain! In contrast, when he placed other rootlets in direct contact with glass, they firmly cemented to the glass after 23 d. He concluded this experiment in these words (p. 106): “…the rootlets first secrete a slightly viscid fluid, subsequently absorb the watery part, and ultimately leave a cement.” We observed a similar type of viscous substance produced by adventitious roots of Adelobotrys adscendens (Melastomataceae) in French Guiana (S. Isnard, personal observation). The exudate cannot be drawn into a thread and remains fluid if removed from the plant. Following Darwin, we kept the drop for several hours, during which period a drop of water would have dried, and then placed the rootlets on a glass plate for a night, after which the rootlet firmly adhered to the glass. Chemical composition of this “viscid fluid” awaits analysis.

Since Darwin’s work, surprisingly few studies have dealt with the adhesive mechanism in climbing plants. Adhesive tendrils of Parthenocissus are known to become swollen at their tips and to flatten against the substrate upon contact, concomitant with a secretion of a cementing substance (Darwin, 1865;Endress and Thomson, 1976; Bowling and Vaughn, 2008). By studying the development of adhesive rootlets in Ficus pumila (syn. F. repens, Moraceae)Groot et al. (2003) also suggested that complete development and adhesion of pads depend upon touch stimuli. A different kind of thigmomorphogenesis occurs if the roots touch moist soil, when they elongate and branch to become nutritive.

The most comprehensive work on vine adhesion has shown that epidermal cells in Parthenocissus quinquefolia become papillate after touch stimulus. Adhesive may be produced from modification and remobilization of wall components of these papillate cells (Bowling and Vaughn, 2008). Immunocytochemichal methods have shown that the adhesive substance is mainly composed of polysaccharides that accumulate at the point of contact between the substrate and the papillate cells (Bowling and Vaughn, 2008). Bowling and Vaughn (2008)proposed that this adhesive becomes lignified and very weather resistant after tendril senescence. Meloche et al. (2004, cited in Core, 2005) found that once securely wrapped around an object, the tendril of redvine (Brunnichia ovata) produces adhesive compounds that cement the tendril in place. Cells enriched with phenols apparently break apart as the tendrils rub against the object.

Hook-climbers

Hook-climbers may include any plants climbing by the aid of recurved spines, hooks, or thorns, which passively assist them in climbing. Hook-climbers are often described as less specialized in that they often lean on the vegetation, but do not firmly attach to the support (Putz, 1984; Putz and Holbrook, 1991;Richards, 1996; Rowe et al., 2006). Darwin (1865) recognized that hook-climbers may not have spontaneous revolving movements. A potential role of light on their growth and development has, however, been suggested. Some hook-climbers grow into shade, which assists finding a support (Darwin, 1865). In Artabotrys hexapetalus (Annonaceae), thorns are correlated with low-light conditions (Posluszny and Fisher, 2000). The most famous hook-climbers are probably the climbing palms from the New and Old worlds, which climb by aid of long “fishing rod-like” structures (Isnard and Rowe, 2008a) derived from leaf (cirrus) or inflorescence (flagellum) (Corner, 1966; Dransfield, 1978) (Fig. 7B). These cirri and flagella bear hooks and acanthophylls (modified leaflets), which are known to be extremely efficient in catching the surrounding vegetation. A single acanthophyll of the South American climbing palms Desmoncus can withstand up to 25 kg before breaking (Isnard and Rowe, 2008a). Putz also noted the efficiency of the attachment in climbing palms. He noted that pulling a stem with a winch exerting a 750 kg force only partly dislodges the established climbing stem. Hooks of climbing palms do not thicken once fixed to a support (Putz, 1990a; Isnard and Rowe, 2008a), but they act as a ratchet-like mechanism where recurved hooks allow a distal sliding but prevent any back movement (Putz, 1990a). By this mechanism, any movement or swing of the climbing axis will bring the stem closer to its support and thus increase the chance of other free attachment devices to encounter and attach. Mechanical measurements have further shown that the strength of hooks increases along the cirrus and flagellum. Thus, climbing palms anchor themselves via the more robust hooks (Isnard and Rowe, 2008a). Slipping from the canopy is, however, common in climbing palms and reflects the ephemeral nature of attachment devices and the lack of branching. New leaves, toward the apex, ratchet on to the vegetation when the stem slips from the canopy, thus renewing anchorage to the supports. The climbing stem can then retain its position in the canopy despite regular slipping.

Self-supporting vs. climbing habit

Liana architecture develops with a “duality” between an initial self-support phase and a later climbing phase (Cremers, 1973, 1974; Caballé, 1986a, b,1998). Liana seedlings typically achieve vertical growth before becoming unstable and climbing onto the surrounding vegetation, via a large diversity of attachment modes. Later in development, shoots of mature lianas that reach the top of the canopy can also be held erect, an advantage for finding and attaching to surrounding supports. Thus, a striking ontogenetic change occurs in stems of many lianas and has a great significance in terms of mechanical and hydraulic function.

An important structural aspect of the transformation to the climbing phase is anatomical. Extensive work on liana wood anatomy by Schenk (1893) and laterObaton (1957) revealed the high frequency of anomalous structure in lianas (Fig. 8). Such structures result from supernumerary cambia or irregular development of the cambium, often followed by a significant development of parenchyma (Schenk, 1893; Obaton, 1957; Caballé, 1986a, 1993; Carlquist, 1991). The complexity of anatomical construction in many lianas is known to arise after the development of climbing architecture (Caballé, 1998). Although some anomalous anatomical organizations are characteristic of family or genus, they cannot be used as a reliable guide to the phylogeny (Schenk, 1893;Obaton, 1957) (Fig. 8). Also, there is apparently no correlation between the type of anomalous structure and attachment mode.

Biomechanics

“Plants become climbers, in order, it may be presumed, to reach the light, and to expose a large surface of leaves to its action and to that of the free air. This is effected by climbers with wonderfully little expenditure of organized matter, in comparison with trees, which have to support a load of heavy branches by a massive trunk.” — Darwin (1865, pp.107, 108)

During the last two decades, studies of functional ecology during growth have highlighted and quantified the contrasting mechanical requirements of self-supporting plants and woody climbers (Gartner, 1991b; Niklas, 1992; Speck, 1994b, a; Rowe and Speck, 1996, 1998, 2004; Speck and Rowe, 1999). Trees have to face an increasing demand in mechanical support (due to increasing weight of the trunk and branches) and exhibit an increase in material stiffness with age. In contrast, lianas rely on their attachment system for their vertical growth and typically decrease in material stiffness with age. The flexural rigidity (stiffness) of stems is characterized by the product of two physically distinct factors: a material stiffness (modulus in bending, similar to Young’s modulus), and a geometric factor (the second moment of area). Because the geometric factor is proportional to the fourth power of stem radius, narrower stems are much more flexible than wider stems of the same material. Of great importance is that climbing plants commonly have a much smaller rate of secondary, radial growth than do trees (Putz, 1983b, 1990b; Ewers et al., 1991). Intuitively, we think of lianas as having more slender stems than do self-supporting trees and thus more flexibility. Flexibility in lianas is often interpreted as a mechanical advantage for a growth form that may hang, swing, or be coiled while slipping or falling from host vegetation.

Besides slenderness (the geometric factor), many complex adaptations have evolved to decrease the material stiffness during development in both monocot and dicot climbers (Fig. 9).

Greater size-normalized flexibility in both twisting and bending are found in old climbing stages of lianas compared to young self-supporting stages (Gallenmüller et al., 2000, 2001). In bending, material stiffness of mature liana stems can indeed be 10 times lower than those of trees: 100–2000 MPa in lianas (Rowe et al., 2006) compared with 5000–14000 MPa for wood of self-supporting species (Niklas, 1992).

Stem stiffness in young stages of growth in lianas is high in the initial self-supporting phase. Besides stem turgor prevailing in primary development, stiffness at this stage is often achieved through (1) secondary xylem with thick-walled fibers and high frequency of narrow vessels or (2) separate bundles or a ring of primary fibers near the periphery of stem section (Fig. 10). This latter organization corresponds to the mechanical hypodermal sterome, a well-developed peripheral zone of the stem consisting of thick walled fiber-shaped cells contributing significantly to the stiffness of the stem (Speck and Vogellehner, 1994; Rowe and Speck, 2004, 2005). Irreversible loss of material stiffness in this type of climber has been shown to result from loss of bundles or rings of primary fibers (i.e., hypodermal sterome) via secondary growth, and the development of wide xylem vessels and large parenchyma rays (e.g.,Clematis, Aristolochia, Passiflora) (Fig. 10C, D) (Speck, 1994a; Isnard et al., 2003; Rowe and Speck, 2005). In climbers with a woody, self-supporting growth phase (e.g., Condylocarpon, Apocynaceae; Strychnos, Loganiaceae;Bauhinia, Caesalpiniaceae; Bignoniaceae sp.), an abrupt change from early wood with thick-walled fibers and high frequency of narrow vessels to late compliant wood, with a higher frequency of large diameter vessels (Fig. 10A, B), causes a drastic reduction of stem stiffness (Rowe and Speck, 1996, 1998,2005; Gallenmüller et al., 2000, 2001; Rowe et al., 2004). This type of functional anatomy (woody vs. hypodermal sterome organization) has potential far-reaching effects on the ecology and evolution of species (Rowe et al., 2004;Rowe and Speck, 2004, 2005). The spatial separation of mechanical and hydraulic functions in the hypodermal liana, where mechanical support relies on primary peripheral tissues, probably permits high hydraulic efficiency of wood, with large diameter vessels, early in the development (Fig. 10C). In contrast, in climbers in which both mechanical and hydraulic functions are combined within wood during the juvenile, self-supporting phase of growth, a potential trade-off between these two functions may constrain water conduction efficiency at this stage.

Besides anatomical adaptations reducing stem stiffness in mature lianas, there are also a number of geometric adaptations. The noncircular geometry of the stem cross-section and the internal organization of tissues, often including compartmentalization of xylem in a soft parenchyma (Fig. 8), are geometrical arrangements that increase stem flexibility (Bhambie, 1972; Fisher and Ewers, 1991; Speck and Rowe, 2003). Anomalous stem anatomies also allow lianas to survive traumatic events after major injuries, by nonfatal splitting of the stem and rapid repair of vascular disruption by wound healing in stems (Fisher and Ewers, 1989, 1991). In addition to having great flexibility, lianas have been shown to sustain large deformation before breaking, a mechanical property known as high toughness. When breaking experiments are conducted on liana stem segments, they typically undergo large plastic deformation beyond their proportional limit of elasticity; sometimes deforming tremendously without breaking. As noted by Putz and Holbrook (1991), if flexibility is undeniably an important attribute of lianas stems, the probability of surviving tree fall might be directly related to their aptitude to survive large deformation without breaking, allowing protection of the vascular system. “Anomalous” structures have long been proposed to allow lianas to function like multistranded cables instead of solid cylinders, following engineering principles and providing both flexibility and toughness (Schenk, 1893; Obaton, 1957; Bhambie, 1972;Carlquist, 1991; Putz and Holbrook, 1991)

In addition to low flexural rigidity and high toughness, lianas exhibit high flexibility during twisting. By applying an angular rotation on liana stem segments connected to a water-filled pressure chamber (0.1 MPa), Putz and Holbrook (1991) demonstrated that a tree sample maintained water flow for less than a single rotation, while most of the lianas revolved several times before flow stopped.

Functional significance of “anomalous” anatomy and stem flexibility in lianas

By comparing different growth forms in western poison oak (Toxicodendron diversilobum, Anacardiaceae), a species that grows as a vine when support is provided but otherwise as a shrub, Gartner (1991a, pp. 2013, 2014) concluded that higher structural stability of shrubs results primarily from the larger diameter of the shrub stem, because “it may be less costly for a plant to achieve a 10-fold increase in flexural stiffness through a 10-fold increase in second moment of area (an increase in transverse area by a factor of 3.2) than through a 10-fold increase in material stiffness.” Higher material stiffness in the shrubby form is less important than geometry in influencing the flexural rigidity. However, the inverse reasoning is not necessarily true. In mature lianas, although slower rates of secondary growth and slender stems contribute to stem flexibility, it can be argued that flexibility is also achieved by low cost reduction of material stiffness, via production of both a large amount of parenchyma (a low cost tissue) and a higher proportion of wide xylem vessels. A synergistic effect on the hydraulic efficiency is evident with this construction (see hydraulics section). Thus, the often-cited trade-off between hydraulic and mechanical functioning in wood of self-supporting species is not evident in lianas. Mechanical investment in mature lianas consists of the protection of the vascular system via stem flexibility and the ability to deform without breaking. Compliant wood and “anomalous anatomy” serve both mechanical and hydraulic functions.

The story, however, is far from simple because, for what appears to be a strikingly efficient conducting system, vulnerability to xylem dysfunction may be particularly critical. In particular, the low vessel turnover rate and the few wide vessels contributing to a disproportionate amount of stem conductivity may render this system quite vulnerable. Moreover, although lianas are well known to support large deformations (Obaton, 1957; Fisher and Ewers, 1991;Putz and Holbrook, 1991), the consequences of these deformations on whole-plant water relations and development remain unknown.

The inner/outer system of secondary growth characterizing many lianas could reflect the contrasting mechanical/hydraulic demands during ontogeny, with (1) an inner cylinder of wood with thick-walled fibers and high frequency of narrow vessels for mechanics of searcher shoot and (2) an outer compliant wood, for hydraulic efficiency, wrapped in a soft parenchyma matrix enhancing mechanical protection of the vascular system. These reflections illustrate the dramatic importance of ontogeny in lianas, which ought to be considered to better understand their ecology and evolution.

In monocotyledons, the stem vascular structure of rattan palms (Calamus) has recently been shown to be unusual among palms. Although vessels are large, water must pass through tiny, irregular vessels (transverse commissures) to flow from one large vessel to another. Then water must pass through a barrier of living cells to reach the leaves. This peculiar vascular construction impedes water transport but has been proposed to minimize cavitation of vessels and/or to be associated with an unknown mechanism of vessels refilling (Tomlinson et al., 2001; Tomlinson and Spangler, 2002). A recent study of this vascular model has shown that the effect of this constriction on the overall water transport is actually small (Cobb, 2006). On the other hand, transverse commissures between vessels have been proposed as a mechanical adaptation for accommodating mechanical strain inherent to the climbing habit (Cobb, 2006).

Type of attachment, mechanical architecture, and trellis requirement

Lianas have many attachment types, which have been extensively used by authors for classification (Darwin, 1865; Putz, 1984; Hegarty, 1991) (see previous section). The type of attachment has been proposed to determine the maximum span between supports and the maximum support diameter (Darwin, 1865; Schenk, 1893; Putz, 1984; Putz and Holbrook, 1991; Rowe et al., 2006). Root-climbers and adhesive pad-climbers can climb the larger support diameters and tendril climbers the smallest (Putz, 1984; Putz and Chai, 1987;Putz and Holbrook, 1991). On the other hand, clinging climbers generally ascend a single support because their mode of attachment requires close contact with a surface to adhere. The type of attachment is also significant in determining the ecology of lianas and their distribution in the different forest successions (Hegarty and Caballé, 1991) and in influencing the mechanical demand a climber has to face throughout its life history (Rowe et al., 2006). Relatively loosely fixed climbers that are attached via hooks undergo quite different mechanical stress and mechanical requirements than do twining lianas fixed tightly to forest trees. Recent studies have shown that developmental changes in stem bending stiffness differ according to the type of attachment to host plants (Rowe et al., 2006). Firmly attached twiners and climbers with tendrils that form a fixed attachment to the host generally have highly flexible mature stems. In contrast, hook- and branch-climbers are more loosely attached to their host vegetation and retain relatively stiff mature stems, probably because the loosely attached stems need stiffness to retain their position in the canopy, whereas firmly attached stems (e.g., twiners and tendril-climbers) are secure by attachment itself. Furthermore, loosely attached stems may unhook, whereas firmly attached stems must survive large deformation during dramatic events (such as a falling support). Interestingly, many facultative climbers and semi-self-supporting species (which simply lean on the surrounding vegetation and do not change in stem material properties with age) are also hook-climbers.

In his monograph on climbing plants, Darwin excluded species that merely scramble over vegetation without any special aids. He described hook-climbers as the least efficient of all climbers. He considered a gradual perfection toward the climbing habit, with tendril and twining climbers being more numerous and having a better climbing mechanism than root- and hook-climbers. These observations are in accordance with mechanical characteristics of different types of climbers where tendril-bearer and twining species generally have more flexible stems, while hook-climbers and scramblers retain relatively stiff stems throughout their lives.

Hydraulics of climbers

Lianas typically have a high ratio of supported leaf weight (and leaf area) to xylem area (i.e., a low Huber value). Hence, if climbing plants represent less than 5% of the aboveground biomass of a tropical forest, they contribute a third or more of total leaf area (Hegarty and Caballé, 1991). In the genus Bauhinia,stems of vine species were found to have not only less xylem per distal leaf area, but also less phloem and cortical tissue than tree or shrub species (Ewers and Fisher, 1991).

Wide and long vessels are common in lianas. Ewers and colleagues (Ewers et al., 1990) found that Pithecotenium crucigerum (Bignoniaceae) can have vessels 7.73 m long. Mean vessel length for 33 species of lianas was 0.38 m, and average maximum length was 1.45 m; maximum vessel width was typically greater than 100 μ (Ewers et al., 1990). Despite greater maximum vessel width in lianas, values for the median vessel dimensions are not necessarily greater than in closely related trees or shrubs (Ewers et al., 1990; Chui and Ewers, 1992), because most of the vessels may be rather short and narrow. According to the Hagen–Poiseuille equation for a system of ideal capillaries, conductivity is proportional to the sum of vessel diameters each raised to the fourth power; therefore, the wider vessels would theoretically conduct a large fraction of the transpiration stream. In the lianas Celastrus orbiculatus (Celastraceae) and Vitis riparia (Vitaceae), larger diameter vessels (>160 µm) are responsible for 63% of the theoretical conductivity, though they only represent 8% of the total vessel in the stem (Tibbetts and Ewers, 2000).

The great maximum width and length of vessels in lianas have long been emphasized and proposed to compensate hydraulically for slender stems by providing a great conductive efficiency. Because conductivity of stem segments depends on the stem cross section, one useful way of scaling conductivity is to divide it by wood area, which yields the specific conductivity, a measure of wood efficiency in conducting water. Empirical measurements, on tropical as well as temperate lianas, have broadly demonstrated that specific conductivity is higher in lianas than in free-standing growth forms, whether closely related species or unrelated species from the same environment are compared (Ewers and Fisher, 1991; Gartner, 1991a; Chui and Ewers, 1992). Similarly, comparative studies on monocotyledons indicate that climbers produce larger diameter and longer vessels than nonclimbers (Tomlinson and Fisher, 2000;Fisher et al., 2002), suggesting greater xylem efficiency to conduct water. Leaf specific conductivity (conductivity divided by leaf area distal to the measured segment, i.e., efficiency of a segment to supply distal leaves with water) of woody, climbing species is not consistently different from those of self-supporting, woody plants (Ewers, 1985; Ewers et al., 1989; Ewers and Fisher, 1991; Gartner, 1991a; Chui and Ewers, 1992). This general result supports the idea that high specific conductivities in lianas compensate for a low ratio of leaf area to xylem area.

Theoretical calculations of conductivity based on vessel diameter overestimate measured flow rates (Ewers et al., 1989; Chui and Ewers, 1992; Tyree and Zimmermann, 2002). The Hagen–Poiseuille equation is based on ideal capillaries and neglects several aspect of water conduction in plants such as the barriers that water has to pass through from one vessel to another (pit membrane and perforation plate), irregularities in vessels walls, or variation of vessels diameter along their length. Pit resistance has been shown to account for >50% of the total xylem hydraulic resistance in many species (Wheeler et al., 2005; Choat et al., 2006). Due to their long vessels, lianas have been proposed to function like ideal capillaries. The few studies on that subject, however, showed that lianas do not function differently from other growth forms, with a measured conductivity (K_h) representing on average less than 50% of the value predicted by Hagen–Poiseuille law (Ewers et al., 1989; Chui and Ewers, 1992;Tyree and Zimmermann, 2002). Recently, we found that the relation between theoretical and empirical conductivity varies with stem development inPassiflora coccinea, with a measured K_h reaching 90–100% of the predicted K_hin old climbing stems (S. Isnard, unpublished data).

Despite the fundamental role of pits in water transport, few anatomists have paid attention to this structure in lianas, and there is a surprising lack of information concerning density of pits or the type of ornamentation. Future research should focus on the microstructure of xylem and functional implications in lianas. Another neglected problem is the capacity for water storage in the transport pathway.

Embolism and liana distribution

Need for research on ecology and global change

Clearly, recent research on climbing plants—habit, development, structure, and function—has filled gaps in Darwin’s seminal work and has greatly extended his wonderful natural history. Intending to follow Darwin’s interests, this review has focused on attachment mechanisms and shoot development and function. But to remain true to Darwin’s enormous breadth of interest in science, it is essential to consider the larger interdisciplinary subjects of ecology and evolution. And indeed in the last two decades, studies of ecology and evolution have, in a certain way, restored the importance of lianas, which have long been neglected in ecological studies. Lianas are now largely known to contribute to many vital aspects of forest dynamics, structure, and composition (Putz, 1983b,1984; Putz and Chai, 1987; Schnitzer and Carson, 2000, 2001; Schnitzer et al., 2000, 2005; Schnitzer and Bongers, 2002; Bongers et al., 2005). More than 133 families of angiosperms contain climbing species (Gentry, 1991), and climbers may represent 10–45% of woody stems in some tropical forests (Putz, 1984;Gentry, 1991; DeWalt and Chave, 2004; Schnitzer et al., 2005). They also comprise as much as 40% of the diversity of woody species (Pérez-Salicrup and Sork, 2001; Schnitzer and Bongers, 2002). Due to their species diversity and abundance in forests, it is now widely admitted that lianas have to be taken into account in silviculture before or after logging (Bongers et al., 2005; Peña-Claros et al., 2008; Putz et al., 2008) as well as in forest vegetation models (Phillips et al., 2002).

Recent reports based on a long-term census from nonfragmented Amazon forests showed that liana abundance is apparently increasing relative to tree species (Phillips et al., 2002; Wright et al., 2004). Authors propose that lianas respond strongly to increasing CO₂ concentration and/or benefit from anthropic perturbation and increasing forest fragmentation (Forseth and Teramura, 1987; Granados and Körner, 2002; Belote et al., 2003;Hättenschwiler and Körner, 2003; Londré and Schnitzer, 2006; Mohan et al., 2006; Zotz et al., 2006). These publications have opened a large debate on the potential societal and economic impacts of increasing vigor and abundance of lianas, particularly in the tropics. A better understanding of the functional ecology and diversity of lianas is therefore an important issue. The diversity of life traits found among lianas indicates that different species may respond differently to environmental changes such as atmospheric CO₂ concentration, forest fragmentation, and changes in tree communities. Thus, there is a great need to study development, physiology, ecology, and functional ecology of climbing plants in response to environmental change.

In the 21st century, we are circling back to Darwin’s comprehensive view of natural history. Contemporary work on climbing plants recognizes the need to integrate biology, geology, and climatology and to achieve understanding of the relationships among cellular, organismal, community, and global size scales.