Mechanical Role of the Leaf Sheath in Rattans

Research

MechanicalBlackwell Publishing Ltd role of the leaf sheath in rattans

S. Isnard1,2 and N. P. Rowe1,2 1Univ Montpellier 2, UMR AMAP Montpellier, F-34000 France; 2CNRS, UMR AMAP Montpellier, F-34000 France

Summary

Author for correspondence: • Leaf sheaths of rattans are long, tubular and persistent and unlike many self- S. Isnard supporting palms, extend far from the apex of the plant. The mechanical role of the + Tel: 04 67 61 75 17 leaf sheath was investigated in eight rattan species of the subfamily Calamoideae. Fax: +04 67 61 56 68 The main objective was to analyse its influence on the mechanical architecture and Email: [email protected] contribution to the climbing habit. Received: 18 July 2007 • Bending mechanical properties were measured along climbing axes before and Accepted: 10 October 2007 after removal of leaf sheaths. Results were related to stem and leaf sheath geometry and mechanical properties. • Contribution of the leaf sheath to axial flexural rigidity was high (c. 90%) in the early stages of growth and towards the apex of older climbing axes for all climbing palms tested. Senescence and loss of the leaf sheath strongly influenced axial stiffness. A nonclimbing species, Calamus erectus, showed a different mechanical architecture. • Although lacking secondary growth, palms have been able to develop successful climbers with a mechanical architecture broadly analogous to, although developmentally different from, dicotyledonous lianas. The role of the leaf sheath in modulating mechanical properties during ontogeny ought not to be neglected in studies on monocotyledons, as it possibly contributed significantly to the ways in which different growth forms have evolved in the group. Key words: architecture, biomechanics, Calamus, climber, leaf sheath, liana, monocotyledons, rattan. New Phytologist (2008) 177: 643–652 © The Authors (2007). Journal compilation © New Phytologist (2007) doi: 10.1111/j.1469-8137.2007.02308.x

Africa. The African rattan clade comprises three endemic Introduction rattan genera (Laccosperma, Eremospatha, and Oncocalamus). Rattan is the common name attributed to spiny Old World Climbers also evolved in the Arecoideae subfamily, but these climbing palms belonging to the Calamoideae subfamily are not generally regarded as true rattans. Climbing species are (Baker et al., 2000), which are found mainly in the genera fewer, with two genera including a single climbing species Calamus and Daemonorops. Calamus (Calaminae, Calamoideae) (Chamaedorea elatior, Dypsis scandens) and a third, Desmoncus, may actually be one of the most successful genera of lianas believed to contain at least seven species (Tomlinson & Fisher, with c. 350 climbing species distributed in tropical forests of 2000; Dransfield et al., 2005). While Desmoncus is widely Southeast Asia (Uhl & Dransfield, 1987). The subfamily also distributed in South America and used for weaving in the contains ‘tree’, shrub and acaulescent palms but is probably western Amazon basin, it lacks the large-scale commercial use best known for its climbers. With 580 climbing species, of its Asian counterparts (Henderson & Chavez, 1993). rattans represent c. 22% of all species of palms. Rattans are Unlike most dicotyledonous lianas, rattans lack secondary widely distributed in Southeast Asia where they are of economic growth, and thus have to maintain their primary-formed importance for the cane-furniture industry (Corner, 1966; vascular system for the entire life of the stem; any mechanical Wickens, 2001). The climbing habit evolved several times damage to the vascular system might therefore be fatal for the within the Calamoideae, mainly in Southeast Asia but also in plant. This is especially true for climbing palms which, for the

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most part, lack the capacity to root and branch (Dransfield, facilitating stem flexibility, whereas in the smaller-bodied 1978). However, despite these apparent constraints, the species, Desmoncus polyacanthos, the leaf sheath remained abundance and species diversity of climbing rattans in many attached to the stem after senescence without significantly tropical forests suggest an ecological and evolutionary success contributing to the mechanical architecture. For both species of this growth form. Rattan palms are particularly interesting studied, stems were stiffer in terms of bending elastic modulus among monocotyledonous climbers for their similarity, in than many previously tested lianas and showed other mechanical terms of size and habitat, to dicotyledonous lianas. They also trends differing markedly from investigated dicotyledonous develop long internodes and possess wider xylem vessels than lianas. In this paper we compare several species of Asian rattans their nonclimbing relatives (Tomlinson et al., 2001), as is often with their potential New Word climbing palm analogue observed in woody lianas (Obaton, 1957; Ewers & Fisher, Desmoncus. This study is part of a project on climbing palms, 1989, 1991). In the manner of lianas, rattans develop long which aims to understand whether the independent origins of stems and, incidentally, rattans are known for developing the the climbing habit in palms is characterized by a diversity of longest aerial stem of any vascular plants, with one measured mechanical architectures and climbing strategies (Rowe et al., climbing stem reaching 200 m in length (Burkill, 1966). Many 2004; Isnard et al., 2005; Isnard, 2006). woody dicotyledonous lianas are well known for producing highly derived variations in stem organization that can drastically Materials and Methods modify the hydraulic and mechanical architecture during the development of the climbing habit, including high specific Stem material conductance and a transition from high stiffness to high flexibility during ontogeny. One of the main objectives of this Four independent sources of material were used. First, wild paper was to assess if the mechanical architecture in rattans material of Calamus acanthospathus Griff. was collected from shows similar characteristics to those of dicotyledonous lianas, secondary forest of South Xishuangbanna county (Yunnan and if so, what those similarities are. province, China), which included seven harvested axes. All scandent palms have slender stems, long internodes, Second, stems of Calamus tetradactylus Hance and Daemonorops and pinnate leaves distributed along the apical portion of the jenkinsiana Mart. cultivated in the Tropical Botanical Garden stem instead of a dense crown of leaves as in most arborescent of Xishuangbanna (XTBG, Yunnan province, China) were palms (Jones, 1995). They are often very spiny and climb with collected (16 and eight stems, respectively). Thirdly, the the aid of specialized organs known as cirri and flagella. The uncommon nonclimbing species Calamus erectus Roxb. was cirrus comprises the whip-like distal extension of the leaf collected in West Yunnan province (Dehong County), from rachis beyond the distalmost leaflets, while the flagellum is an which six axes were tested. These three collections provide elongated, unbranched and sterile inflorescence (Corner, 1966; the most detailed information in this study. Fourthly, one Dransfield, 1978). These specialized attachment structures, to three stems each of C. australis Mart., C. caesius Blume, functioning as grapnels, are very efficient and it is often difficult, if C. caryotoïdes A. Cunn and C. longipinna K. Schum were studied not impossible, to dislodge well established rattan stems (Putz, from the Palm House of the Royal Botanic Gardens (Kew, UK). 1990). A particularly interesting feature of climbing palms is their tubular and persistent leaf sheath, which firmly encircles Study site the cane along a significant part of the stem length. This contrasts with the shorter leaf sheath of many self-supporting palms, Although not close to the equator, Yunnan province (southwest confined to the crown (Tomlinson, 1962). From a mechanical China) possesses a rich tropical flora and lowland tropical perspective, the presence of a thick leaf sheath surrounding forests (Zhu & Cai, 2004). The flora is estimated to contain the stem in climbing palms significantly affects their mechanical c. 36 321 species (one-seventh of the Chinese flora) belonging architecture, at least during part of their growth trajectory. In to 197 families. Xishuangbanna county (21°10′–22°40′N this paper we investigate how the morphology and development latitude), in southern Yunnan, is one of nine autonomous of the leaf sheath influence the mechanical architecture of rattans prefectures of Yunnan and is home to c. 33 native rattan and how it contributes to the climbing habit. For this purpose, species. The mean annual temperature is 21.5°C and the we carried out geometrical and biomechanical analyses on seven rainfall is 1560 mm. The Xishuangbanna Botanical Tropical climbing rattan species and, for the sake of comparison, a self- Garden is located in western Xishuangbanna, and covers an supporting rattan species in which the leaf sheath is shorter area of 900 ha, including 10 000 cultivated species; this is the and limited to the crown. largest botanical garden in China. A recent study of the South American climbing palm Desmoncus has shown that the mechanical role of the leaf Mechanical tests sheath varies between species, and differs with size and habitat (Isnard et al., 2005). Loss of the leaf sheath with age was The objective of these tests was to determine the flexural observed for a large size species, Desmoncus orthacanthos, thus rigidity, EI, of intact axes, that is, entire stem segments with

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Fig. 1 Morphology of leaf sheaths in rattans. (a) Young stem of Calamus tetradactylus with tubular leaf sheath encircling the cane; (b) transverse section of a young axis of the climbing species Daemonorops jenkinsiana showing the typical organization of the cane and surrounding leaf sheaths; (c) local fracture of leaf sheaths in D. jenkinsiana resulting from excessive bending stresses and exposing the flexible cane; (d) basal portion of an old climbing stem of C. acanthospathus forming coils on the forest ground; (e) deeply split and nonpersistent leaf sheath in the nonclimbing species C. erectus. f, flagellum; ls, leaf sheath; p, petiole. their leaf sheaths, and that of stems without their leaf sheaths. values were then calculated for both directions and the final For the latter case, the leaf sheaths were carefully removed radius was calculated from the mean values of these two with a knife. Three-point bending tests were carried out on directions. The degree of tapering was below 10% of the segments with the leaf sheath intact and manually removed calculated mean diameter for the three positions along each for all the species included in the study. Furthermore, for the tested specimen. two species C. acanthospathus and C. tetradactylus, canes of older climbing stems were measured from which the leaf sheaths Results had been lost naturally. Bending test protocols followed those used in previous studies (Vincent, 1990; Isnard et al., 2005). Leaf sheath morphology and development Stem segments, cut along the plant, were placed horizontally on two vertical supports, and consecutive weights added at the Free-standing juvenile axes of rattans are characterized by a centre of the tested segment. The resulting vertical deflection thick, tubular, persistent leaf sheath firmly surrounding the of the stem was measured via a dissecting microscope. The cane (Fig. 1a,b). The petiole, which develops from the leaf flexural rigidity (N mm2) of each segment was calculated sheath, emerges two to three internodes above its insertion using the formula EI = L3/48R, where L is the length of the point, and two to three leaf sheath layers consequently encircle tested stem segment (distance between the two vertical supports), the cane at any position along the plant. The external layer is and R is the slope of the best-fitting regression curve of the often thicker and densely armed with long and stiff spines. force plotted against deflection (Δdeflection (mm)/Δforce The leaf sheath remains intact and green after the palm has (N)). Here, E (MPa) is Young’s modulus, a measure of the located a support and started to climb, and remains so in the material stiffness in bending. I (mm4) is the second moment apical portion of long climbing stems. Intact leaf sheaths bear of area, a measure of the contribution of cross-sectional area, the attachment devices, cirri or flagella in Calamus (Fig. 1a) and geometry, and shape to the ability to resist bending forces cirri in Daemonorops. The radial thickness of the leaf sheaths (Niklas, 1992). The I of each segment is calculated using the varies with age and degree of senescence, and measurements formula I = 0.25πa3b, where a and b represent the radial were consequently done on green and intact leaf sheaths along width in the direction of, and perpendicular to, the applied the length of the entire plant. Despite the diversity in leaf force, respectively. sheath thickness among species, all the rattans studied exhibit Measurements of leaf sheath radial thickness were obtained a quite homogeneous contribution of the leaf sheath to the by subtracting the cane radius from the total radius of cane total axial diameter, with values ranging from 30 to 40% plus leaf sheath. Diameters were taken in two directions (a and (Table 1). The geometric contribution to the flexural rigidity b) and in three positions along the tested segments. Mean of stems (leaf sheath’s second moment of area) is significantly

Table 1 Geometric contribution of the leaf sheath in five rattan species

Contribution to Species Radial thickness (mm) axes diameter (mm) Contribution to I (%)

Calamus acanthospathus (n = 40) 2.7 ± 0.9 34.0 ± 3.1 80.7 ± 3.4 Calamus caesius (n = 5) 2.1 ± 0.3 41.6 ± 3.8 88.6 ± 3.2 Calamus longipinna (n = 9) 2.3 ± 0.5 30.5 ± 3.3 77.6 ± 4.1 Calamus tetradactylus (n = 74) 1.8 ± 0.4 37.9 ± 5.1 85.3 ± 4.6 Daemonorops jenkinsiana (n = 34) 5.1 ± 0.7 36.6 ± 3.7 83.1 ± 3.9

Values are means ± 1 SD.

more important, with values > 70%. This result emphasizes The contribution of leaf sheaths to stem flexural rigidity the potential mechanical significance of the outer leaf sheath has been calculated for plants whose green and intact leaf sheath ring for structural support of the plant, especially in early has been manually removed (Fig. 2c). For all species tested the stages of growth. Field observations have revealed that the leaf contribution is high, > 90%. This demonstrates a significant sheath may break locally as a result of excessive mechanical mechanical function of the leaf sheath in contributing to the stress after rattans fall from their support. The failure of the ability of juvenile axes and the apical portion of climbing axes leaf sheath results in a local deformation of the more flexible cane to resist bending forces. inside (Figs 1c), but does not seem to affect the plant growth. In all species studied that had developed to maturity, the Mechanical architecture of climbing axes leaf sheath senesces and is progressively loosened towards the base of old climbing axes, resulting in flexible canes which The mechanical architecture of mature climbing axes was form long loops on the forest floor (Fig. 1d). Interestingly, in studied in two species of Calamus, C. acanthospathus and the nonclimbing rattan species, C. erectus, the leaf sheath is C. tetradactylus, for which leaf sheaths had been naturally lost not persistent but rapidly dries below the apex. Contrary to towards the base. Values of flexural rigidity (EI) and Young’s climbing species where the leaf sheath is tubular, leaf sheaths modulus (E) are plotted against distance from the base of of C. erectus are deeply split longitudinally and do not entirely individual plants as double logarithmic plots (Fig. 3). Both cover the stem (Fig. 1e). species show a similar trend along axes with a drastic increase in rigidity along portions of stems where leaf sheaths encircle the cane (Fig. 3a). Long and flexible canes, lacking a leaf A survey of flexural rigidity for eight rattan species sheath and lying along the ground or hanging from the forest Flexural rigidity is plotted against axial diameter to demonstrate canopy, show relatively constant values of flexural rigidity variations of size and rigidity among species. Selected species along their length. The apical portions of stems surrounded indeed represent a large size range, from 6 to 40 mm in by green and intact leaf sheaths range between 3 and 8 m in diameter, with Daemonorops jenkinsiana the largest of the length. This corresponds to the portion of the plant bearing climbing species tested. Calamus erectus, a nonclimbing rattan the attachment devices (flagella or cirri) and anchored to the of the Calaminae subtribe, is represented in the second plot surrounding vegetation. (Fig. 2b), since the species does not exhibit an intact tubular A drastic increase in Young’s modulus, several metres below leaf sheath even in young stages of growth. Leaf sheaths in this the shoot apex, is also associated with the presence of green species are only present toward the apex of the stem over a and intact leaf sheaths bearing cirri or flagella (Fig. 3b). The short length, which cannot be measured in bending. Young’s modulus increases from values of below 4000 MPa As expected, due simply to the significant role of size to along canes to values of 8000–10 000 MPa in distal parts of stem mechanics, the larger diameter species exhibit the higher the plant. However, contrary to the pattern observed for flexural flexural rigidity (Fig. 2a). Logarithmic increase in rigidity rigidity, the Young’s moduli tend to increase somewhat with overall diameter follows the same slope for all the species. proximally along canes. The decrease in both flexural rigidity In all the climbing species, flexural rigidity decreases by at and Young’s modulus towards the very apex, observed for all least one order of magnitude after the leaf sheath has been stems, is readily explained by the juvenile state of the apical naturally lost in old stems (i.e. canes) or manually removed shoots and tissue immaturity. (juvenile stems) (Fig. 2b). Flexural rigidity of C. erectus segments A detailed analysis of Young’s modulus variations along is at least two orders of magnitude higher than that of the juvenile and mature canes (i.e. the axis without leaf sheaths) climbing species. Stem rigidity in C. erectus is even higher than for two species of rattan is shown in Fig. 4. Juvenile axes of that in juvenile and stiff stems of climbing species whose thick C. acanthospathus and C. tetradactylus that do not exceed 5 m leaf sheaths still encircle the stem. and where leaf sheaths have been manually removed, show an

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Fig. 2 Double logarithmic plot of flexural rigidity against diameter for eight rattan species (seven climbing species and the nonclimbing Calamus erectus). (a) Juvenile axes with their leaf sheaths; (b) canes and juvenile stems after removal of leaf sheaths; (c) mean contribution (±1 SD) of leaf sheaths to the total flexural rigidity (EI) of young axes and distal segments of climbing stems. n, number of tested segments. increase in Young’s modulus toward the base (Fig. 4a,b). This consequently, underline the fact that the mechanical contribution pattern is typical of self-supporting growth forms of many of leaf sheaths to flexural rigidity is not only geometric plants, where elastic modulus increases basally. The same (because of its contribution to the axial second moment of trend in material properties is observed for old climbing area), but also explained by tissue stiffness. Values for canes are stages, with stem lengths ranging from 10 to 70 m. Values of lower and c. 2000 MPa for the two tested climbing species, Young’s modulus towards the base of old stages of growth are C. acanthospathus and C. tetradactylus. For these two species, slightly higher than those measured towards the base of young the mean E of young stems where leaf sheaths have been axes, suggesting late tissue maturation and stiffening of the manually removed is lower than that of mature canes, where cane. the leaf sheaths have been lost naturally with age. However, Mean values of Young’s modulus for all the species included the difference is not significant and this suggests that bending in the study are shown in Table 2. The results emphasize high measurements of stems after manually removing the leaf sheaths values of Young’s modulus for stems with their leaf sheath and, provide a good approximate value of the Young’s modulus

Table 2 Mean values of Young’s modulus (E, MPa) for three types of axial segment of rattan (Calaminae, Calamoideae)

E (MPa) of stems with E (MPa) of stems with Species leaf sheaths leaf sheaths removed E (MPa) of stems (= canes)

Calamus tetradactylus 7013 ± 1606 1624 ± 705 2293 ± 515 Calamus acanthospathus 6097 ± 1728 1273 ± 474 1912 ± 632 Calamus caryotoïdes 7941 ± 2277 2272 ± 791 − Calamus longipinna 6793 ± 1509 1027 ± 318 − Daemonorops jenkinsiana 6632 ± 1327 1985 ± 548 − Calamus australis 5115 ± 1767 −− Calamus caesius 4441 ± 1074 −− Calamus erectus −−11 358 ± 930

Values are means ± 1 SD.

to the ability of stems to resist bending forces is high, and > 90% in juvenile stages of growth and apical portions of climbing stems attached to the surrounding vegetation or searching for supports. This important contribution of the leaf sheath to flexural stiffness is the result of both its peripheral position (its axial second moment of area) and its material properties (Young’s modulus). This differs markedly from the two Desmoncus species studied previously, where the contribution of the leaf sheath reached only c. 54% for D. polyacanthos and 76% for D. orthacanthos (Isnard et al., 2005). Moreover, the mechanical contribution of the leaf sheath to stem flexural rigidity is essentially geometric for the South American species of Desmoncus, as the Young’s modulus of leaf sheaths is actually lower than that of the canes (Isnard et al., 2005). An increase in flexural rigidity from the mature cane to the more apical zone of stem with surrounding leaf sheaths, observed in the detailed study of C. acanthospathus and C. tetradactylus, would probably apply to other Calamoideae tested from glasshouse material that were only represented by relatively young stages of growth, since loss of leaf sheath Fig. 3 Mechanical properties along climbing axes for two rattan would definitely lead to a significant reduction of axial second species (Calamus acanthospathus, open circles; C. tetradactylus, moment of area, and the Young’s modulus of tested canes closed circles). The arrows indicate the position above which the green leaf sheath surrounds the stem. (a) Flexural rigidity; (b) Young’s (after manually removing the leaf sheath) was always found to modulus. be significantly lower than that of entire axes in all tested species. A drop in flexural rigidity towards the base of long climbing stems has also been observed for the large-size stems of mature canes. While all the climbing species studied display of Desmoncus species, but to a lesser degree (Isnard et al., a Young’s modulus of cane ranging between 1000 and 2005). This is readily explained by the much larger values of 2300 MPa, the nonclimbing species C. erectus exhibits very Young’s modulus of the stem compared with values measured stiff stems with a mean Young’s modulus of c. 11 000 MPa, in Calamus and Daemonorops species (Table 3). five times greater than canes of climbing species. The development and senescence of the leaf sheath along climbing axes strongly influence the mechanical architecture of rattans during their growth and establishment. Senescence Discussion and shedding of leaf sheaths with age do, indeed, lead to a drastic loss of rigidity towards the base of old stems. Leaf Leaf sheath and mechanical architecture of sheaths may also break naturally under excessive mechanical climbing palms stresses (bending and torsion) and the flexible underlying canes Thick and persistent leaf sheaths play an important mechanical thus easily bend or twist, complying with environmentally role in rattans. In all tested species, contributions of leaf sheaths induced deflections without breaking. Breakage might be

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Fig. 4 Young’s modulus (MPa) along canes for two climbing species. (a, b) Juvenile stages of growth where leaf sheath has been manually removed before bending tests; (c, d) old climbing stems where leaf sheath has been manually removed only towards the apex.

Table 3 Young’s moduli of climbing palms and selected dicotyledonous lianas

E (MPa) Young stage E (MPa) Old stage Sources

Climbing palms Calamus acanthospathus 6110 ± 1560 1830 ± 670 Calamus tetradactylus 7070 ± 1560 2300 ± 500 Daemonorops jenkinsiana 6630 ± 1330 1990 ± 500 Plectocomia himalayana 3340 ± 860 4300 ± 570 Isnard (2006) Desmoncus polyacanthos 3200 ± 2060 8090 ± 2500 Isnard et al. (2005) Desmoncus orthacanthos 4000 ± 1070 8900 ± 2200 Isnard et al. (2005) Dicotyledonous lianas Aristolochia macrophylla 2470 ± 480 500 ± 390 Speck et al. (1997) Clematis vitalba 3070 ± 1080 770 ± 260 Isnard et al. (2003) Maripa scandens 4110 ± 510 390 ± 30 Rowe et al. (2006) Passiflora glandulifera 4540 ± 620 630 ± 130 Rowe et al. (2006) Condylocarpon guianensis 2720 ± 900 310 ± 50 Rowe & Speck (1996) Bauhinia guyanensis 8480 ± 2820 350 ± 100 Rowe & Speck (1998)

Values are means ± 1 SD.

induced by movements or falls from the supports or slipping surrounding vegetation via relatively few apical leaves, and of the rattan stem from the canopy. Indeed, senescence of the therefore relatively few anchorage points, which occasionally leaf sheath is accompanied by the decay and progressive loss leads to the stems slipping off the canopy (Corner, 1966; Putz, of attachment devices, resulting in the unhooking of this portion 1990). Flexible canes thus seem to be mechanically adapted to of the stem. Long climbing stems are often attached to the form loops on the ground rather than breaking.

Finally, we suggest that leaf sheath/cane organization in slightly increases basally in rattans; this increase is slight, rattans might be interpreted as mechanical adaptation, allowing however, compared with the proximal increase in elastic modulus climbers to be stiff enough in the early stages of growth to observed in canes of the two Desmoncus species previously reach supports and maintain their position in the canopy, and tested (Isnard et al., 2005). Differences in stem material to become extremely compliant with age or after external properties between Desmoncus and true rattans are readily mechanical stresses. Interestingly, these mechanical adaptations observed by differences in anatomical organization (Rowe et al., are not observed at all for one of the rare nonclimbing rattan 2004). In Desmoncus, very dense bundles with thick-walled members, C. erectus. Stems of this species are very rigid, owing fibres are distributed at the periphery of the stem, and the to both the stem stiffness and the larger diameter, and leaf number of bundles and their density decrease toward the centre sheath morphology and development are more typical of of the stem cross-section (Tomlinson & Zimmermann, 2003). arborescent palms. This kind of organization has been observed in arborescent palms, where stiffness is concentrated at the periphery of the stems and increases towards the base of the stem (Rich, 1986, Achieving compliance without secondary growth 1987). Rattans, however, show distinctive peripheral bundle A well-known trend in dicotyledonous lianas is a decrease in density, and the well-developed and dense system of fibres Young’s modulus from the apex of the stem to its base (Putz observed in most palms is not as pronounced (Tomlinson & Holbrook, 1991; Speck, 1994; Rowe & Speck, 1996). This et al., 2001). differs markedly from the trends characterizing self-supporting In most monocotyledons, the basal part of the leaf forms a species where Young’s modulus generally increases with age sheath which encircles a portion of the stem just above the towards the base of stems. As a consequence, liana stems are node where the leaf is attached (Holttum, 1955). The sheaths much more flexible than equivalent diameter stems of self- generally mature before the juvenile internodes they envelop supporting species. Greater flexibility in old stages of growth and provide a mechanical strengthening to the stem (Niklas, in lianas is often interpreted as a way to limit or prevent damage 1992). Our study provides a new insight into the mechanical to which the stem might suffer when slipping or falling from role of the leaf sheath in climbing palms, showing that this a support. This flexibility in dicotyledonous lianas is often structure may modulate mechanical properties of the axis. achieved through so-called ‘anomalous’ secondary growth The functional role of the leaf sheath consequently ought not (Obaton, 1957; Fisher & Ewers, 1989, 1991; Isnard et al., to be neglected in monocotyledons as it might potentially 2003; Rowe & Speck, 2004). From this point of view, contribute significantly to the ways in which different growth monocotyledonous climbers lacking secondary growth may forms have evolved in the group. be constrained in the degree to which they can modulate material properties of the stem during growth and in Evolutionary success response to the environment or extrinsic mechanical constraints. Our results on climbing palms show that some A detailed developmental study of arborescent palms by Rich monocotyledonous climbers are nevertheless able to (1986, 1987) indicates that palms maintain their safety margin drastically change their stem stiffness during growth and against mechanical failure because of sustained lignification, establishment, via their leaf sheath. Comparisons of especially at the stem periphery and stem base (Rich, 1986). mechanical properties of dicotyledonous lianas and climbing The mechanical architecture of arborescent palms shows a palms (Table 3) provide an interesting insight into the fact drastic increase in stem stiffness and strength during increase that rattans exhibit a broadly similar mechanical trend to in height, with the elastic modulus being greatest toward the dicotyledonous lianas. Values of Young’s modulus of rattan stem periphery and base. canes are, however, relatively high and among the higher Recent studies on the South American genus Desmoncus values of old growth stages of lianas previously tested suggest that the genus actually develops a similar mechanical (Table 3). But greater flexibility of cane in rattans is achieved architecture as arborescent palms in terms of an increase in by small cane diameter (3–20 mm). Young’s modulus towards the base (Isnard et al., 2005); and Conversely, the trends observed in species of the South shares the basic stem organization of the Raphis model American palms Desmoncus are analogous to those of self- (Tomlinson & Zimmermann, 2003). These observations supporting species that show an increase in Young’s modulus differ from those found in rattan palms (e.g. Calamus), in which with age. This study has revealed an unusual mechanical recent research on the hydraulic architecture has revealed an pattern in monocotyledonous species, where the Young’s unusual vascular construction compared with those of modulus of old climbing axes decreases towards the base of the arborescent palms (Tomlinson et al., 2001, Tomlinson & plant, caused by loss of the leaf sheaths. We note here that Spangler, 2002). The most distinctive stem structural feature Young’s modulus is measured along climbing stems, where the emphasized by authors is ‘the method of origin of axial leaf sheath is lost towards the base but still encircles the apical bundles, which are never branches of an outgoing leaf trace, portion of the stem. Along the cane only, Young’s modulus but arise by axial differentiation of a procambial strand’.

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Moreover, Calamus does not have a bridge system as In: Putz FE, Mooney HA, eds. The biology of vines. Cambridge, UK: described in the Raphis model, but axial connections via Cambridge University Press, 99–124. commissures (Tomlinson & Spangler, 2002). Finally, it has Henderson A, Chavez F. 1993. Desmoncus as a useful palm in the Western Amazon basin. Principes 37: 184–186. also been proposed that vessels are less specialized in Raphis Holttum RE. 1955. Growth-habits of monocotyledons-variations on a and Desmoncus (scalariform perforation plates) compared theme. Phytomorphology 5: 399–413. with Calamus (simple perforation plates) (Tomlinson & Isnard S. 2006. Biomechanics and development of rattans: what is special Zimmermann, 2003). about Plectocomia himalayana Griff. (Calamoideae, Plectocomiinae)? In addition to this, our data suggest an unusual mechanical Botanical Journal of the Linnean Society 151: 83–91. Isnard S, Speck T, Rowe NP. 2003. Mechanical architecture and architecture in rattans that differs from that of the South development in different growth forms of Clematis: implications American climbing palm Desmoncus. The study also supports for canalised evolution of growth forms. New Phytologist 158: the idea (Rowe et al., 2004) that the mechanical architecture 543–559. of rattans is adapted to an arguably more specialized climbing Isnard S, Speck T, Rowe NP. 2005. Biomechanics and development habit, where a higher degree of flexibility of the stem after of the climbing habit in two species of the South American Palm genus Desmoncus (Arecaceae). American Journal of Botany 92: 1444–1456. loss of the leaf sheath can protect the plant against irre- Jones DL. 1995. Palms throughout the world. Sydney, Australia: New Holland versible mechanical damage. These mechanical and vascular Publishers. peculiarities are possibly implicated in the evolutionary success Niklas KJ. 1992. Plant biomechanics: an engineering approach to plant form of rattans and might have contributed to the great diversity of and function. Chicago, IL, USA: University of Chicago press. species. Obaton M. 1957. Les lianes ligneuses à structure anormale des forêts denses d’Afrique occidentale. Paris, France: Doctorat és Sciences Naturelles, Faculté des Sciences. Putz FE. 1990. Growth habits and trellis requirements of climbing palms Acknowledgements (Calamus spp.) in north-eastern Queensland. Australian Journal of Botany This work was supported by a grant to SI from the Agence 38: 603–608. Universitaire de la Francophonie (AUF) (France). We thank Putz FE, Holbrook NM. 1991. Biomechanical studies of vines. In: Putz FE, Mooney HA, eds. The biology of vines. Cambridge, UK: Cambridge Chen Jin, Hu Jian-Xiang and colleagues from Xishuangbanna University Press, 73–97. Tropical Botanical garden (Yunnan Province, China) for Rich PM. 1986. Mechanical architecture of arborescent rain forest palms. assistance with this project. We also acknowledge Bill Baker Principes 30: 117–131. and John Dransfield from the Royal Botanic Gardens, Kew for Rich PM. 1987. Developmental anatomy of the stem of Welfia georgii, discussion and for generously authorizing collection of rat- Iriartea gigantea, and other arborescent palms: implications for mechanical support. American Journal of Botany 74: 792–802. tans from the palm house. Finally, we thank Paula Rudall at Rowe NP, Isnard S, Gallenmüller F, Speck T. 2006. Diversity of mechanical the Jodrell Laboratory, for generously affording us labora- architectures in climbing plants: an ecological perspective. In: Herrel A, tory facilities for the measurements at Kew. Speck T, Rowe NP, eds. Ecology and biomechanics: a mechanical approach to the ecology of animals and plants. Boca Raton, FL, USA: CRC Press LLC, 35–59. References Rowe NP, Isnard S, Speck T. 2004. Diversity of mechanical architecture in climbing plants: an evolutionary perspective. Journal of Plant Growth Baker WJ, Hedderson TA, Dransfield J. 2000. Molecular phylogenetics Regulation 23: 108–128. of Calamus (Palmae) and related rattan genera based on 5S nrDNA Rowe NP, Speck T. 1996. Biomechanical characteristics of the ontogeny and spacer sequence data. Molecular Phylogenetics and Evolution growth habit of the tropical liana Condylocarpon guianense (Apocynaceae). 14: 218–231. International Journal of Plant Sciences 157: 406–417. Burkill IH. 1966. A dictionary of the economic products of the Malay Rowe NP, Speck T. 1998. Biomechanics of plant growth forms: the Peninsula. Kuala Lumpur, Malaysia: Ministry of Agriculture and trouble with fossil plants. Review of Palaeobotany and Palynology Cooperative. 102: 43–62. Corner EJH. 1966. The natural history of palms. Berkeley, CA, USA: Rowe NP, Speck T. 2004. Hydraulics and mechanics of plants: novelty, University of California Press. innovation and evolution. In: Poole I, Hemsley AR, eds. The evolution of Dransfield J. 1978. Growth forms of rain forest palms. In: Tomlinson PB, plant physiology. Kew, UK: Elsevier Academic Press, 297–325. Zimmermann MH, eds. Tropical trees as living systems. New York, NY, Speck T. 1994. A biomechanical method to distinguish between self- USA: Cambridge University Press, 247–268. supporting and non self-supporting fossil plants. Review of Dransfield J, Uhl NW, Asmussen CB, Baker WJ, Harley MM, Lewis CE. Paleobotany and Palynology 81: 65–82. 2005. An outline of a new phylogenetic classification of the palm family, Speck T, Neinhuis C, Gallenmüller F, Rowe NP. 1997. Trees and shrubs in Arecaceae. Kew Bulletin 60: 559–569. the mainly lianescent genus Aristolochia s.l.: secondary evolution of the Ewers FW, Fisher JB. 1989. Variation in vessel length and diameter in self-supporting habit? In: Jeronimidis G, Vincent JFV, eds. Plant stems of six tropical and subtropical lianas. American Journal of Botany biomechanics. Reading, UK: University of Reading, 201–208. 76: 1452–1459. Tomlinson PB. 1962. The leaf base in palms its morphology and mechanical Ewers FW, Fisher JB. 1991. Why vines have narrow stems: histological biology. Journal of the Arnold Arboretum 43: 23–45. trends in Bauhinia (Fabaceae). Oecologia 88: 233–237. Tomlinson PB, Fisher JB. 2000. Stem vasculature in climbing Fisher JB, Ewers FW. 1989. Wound healing in stems of lianas after twisting monocotyledons: a comparative approach. In: Wilson KL, Morrison DA, and girdling injuries. Botanical Gazette 150: 251–265. eds. Monocots: systematics and evolution. Melbourne, Australia: CSIRO Fisher JB, Ewers FW. 1991. Structural responses to stem injury in vines. Publishing, 89–96.

Tomlinson PB, Fisher JB, Spangler RE, Richer RA. 2001. Stem vascular Uhl NW, Dransfield J. 1987. Genera Palmarum: A classification of palms architecture in the rattan palm Calamus (Arecaceae-Calamoideae- based on the work of Harold E. Moore, Jr. Lawrence, KS, USA: Allen Press. Calaminae). American Journal of Botany 88: 797–809. Vincent JFV. 1990. Structural biomaterials. Princeton, NJ, USA: Princeton Tomlinson PB, Spangler RE. 2002. Developmental features of the University Press. discontinuous stem vascular system in the rattan palm Calamus Wickens GE. 2001. Timber and wood production. Economic botany: (Arecaceae-Calamoideae-Calamineae). American Journal of Botany principles and practices. Dordrecht, the Netherlands: Kluwer Academic 89: 1128–1141. Publishers. Tomlinson PB, Zimmermann MH. 2003. Stem vascular architecture in the Zhu H, Cai L. 2004. Vegetation of upper Mekong valley. Mankind and American climbing palm Desmoncus (Arecaceae-Arecoideae-Bactridinae). nature, Supplement 7. Kunming, China: Yunnan Education Publishing Botanical Journal of the Linnean Society 142: 243–254. House.

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