Developmental plasticity and biomechanics of treelets and lianas in Manihot aff. quinquepartita (Euphorbiaceae): a branch-angle climber of French Guiana

Abstract

Background and aims: Most tropical lianas have specialized organs of attachment such as twining stems, hooks or tendrils but some do not. Many climbers also have an early self-supporting phase of growth and in some species this can produce treelet-sized individuals. This study focuses on how a liana can climb without specialized attachment organs and how biomechanical properties of the stem are modulated between self-supporting treelets and canopy-climbing lianas.

Methods: Biomechanics and stem development were investigated in self-supporting to climbing individuals of Manihot aff. quinquepartita (Euphorbiaceae) from tropical rain forest at Saül, central French Guiana. Bending tests were carried out close to the site of growth. Mechanical properties, including Young's elastic modulus, were observed with reference to habit type and changes in stem anatomy during development.

Key results: This liana species can show a remarkably long phase of self-supporting growth as treelets with stiff, juvenile wood characterizing the branches and main stem. During the early phase of climbing, stiff but unstable stem segments are loosely held in a vertical position to host plants via petiole bases. The stiffest stems--those having the highest values of Young's modulus measured in bending--belonged to young, leaning and climbing stems. Only when climbing stems are securely anchored into the surrounding vegetation by a system of wide-angled branches, does the plant develop highly flexible stem properties. As in many specialized lianas, the change in stiffness is linked to the development of wood with numerous large vessels and thin-walled fibres.

Conclusions: Some angiosperms can develop highly effective climbing behaviour and specialized flexible stems without highly specialized organs of attachment. This is linked to a high degree of developmental plasticity in early stages of growth. Young individuals in either open or closed marginal forest conditions can grow as substantial treelets or as leaning/climbing plants, depending on the availability of host supports. The species of liana studied differs both in terms of development and biomechanics from many other lianas that climb via twining, tendrils or other specialized attachment organs.

Fig. 1.

Growth forms of Manihot aff. quinquepartita: (A) young self-supporting individual over 1 m high in gap conditions of disturbed secondary forest; (B) young individuals leaning against branches of neighbouring vegetation; at this stage of development stems are relatively loosely ‘attached’ to the supports via petiole bases; (C) young climbing individuals over 6 m long, well into the climbing phase of development and anchored in the branches of the host trees; (D) self-supporting treelet, 3 m in height, in open gap conditions of disturbed secondary forest; (E) evidence of thigmo-response of leaf petioles; note the angle of the petiole to the upper left of the stem compared with the reflexed orientation of the two petioles interacting with the narrow branch; (F) mature climbing liana producing pendulous axes bearing immature fruits (April 2006) in openings between adjacent plant hosts – fruiting specimens were only observed on mature climbing individuals.

Fig. 2.

Growth forms of climbing Manihot aff. quinquepartita. (A) Large-bodied mature liana. The base of the main stem (lower left) extends to the right, producing numerous branches, which are irreversibly anchored into the vegetation above. This organization is quite unlike that of aged self-supporting individuals. (B) Wide-angled branches of mature climbing individual. Such branches act as highly effective grappling hooks in host vegetation. Plants that have developed this degree of branch attachment cannot be removed from the canopy.

Fig. 3.

(A) Young's elastic modulus measured in three-point bending, plotted against stem diameter for the three main types of growth form – self-supporting, leaning and climbing. All growth form categories increase in stiffness with increasing stem diameter up to about 10 mm diameter. After this point, larger self-supporting stems retain high values of E, whereas equivalent diameter climbing plants are more flexible. (B) Pair-wise comparisons of elastic moduli for self-supporting and climbing growth forms. Self-supporting and climbing stem classes are grouped in terms of stem diameter: 1, <5·4 mm; 2, 5·5–7·4 mm; 3, 7·5–10·5 mm; 4, > 10·5 mm. Only the largest and oldest category (>10·5 mm) shows statistical significance between median values of E for self-supporting and climbing stem stiffness (P < 0·01, Mann–Whitney test).

Fig. 4.

(A) Young's elastic modulus measured in bending plotted against the percentage contribution of the wood cylinder to the total cross-sectional area of each tested stem. Generally, in all growth forms, the modulus increases with increasing proportion of wood surface area, except for a group of older climbing stems between 38 % and 56 % contribution which have relatively low wood contributions coupled with low modulus values. (B) Young's elastic modulus measured in bending plotted against the percentage contribution of the cortex to the total cross-sectional area of each stem tested. There is a general decrease in modulus with increasing proportion of cortical tissues. (C) Young's elastic modulus measured in bending plotted against the percentage contribution of the wood to the total second moment of area of each tested stem. In general, stems increase in stiffness with increasing contribution of the wood to second moment of area (I). Interestingly, for a given value of percentage wood contribution to I, the stiffest stems [the upper cloud of points increasing in stiffness (E) towards the right] belong mostly to young climbing stems (<10 mm in diameter) that are lightly attached to vertical supports.

Fig. 5.

Transverse section surfaces showing macroanatomical development in M. aff. quinquepartita. In all sections the central white area is pith; the black arrow marks the outer limit of the juvenile wood and the white arrow marks the outer limit of the adult lianoid wood. (A) Large, self-supporting stem with narrow pith, homogeneous, dense, stiff wood and narrow band of cortical tissues and bark. This kind of organization is typical of large self-supporting shrub-like stems growing in the absence of supports. (B) Mature climbing stem showing a narrow pith, a band of dense juvenile wood and abrupt transition to less dense wood with abundant large-diameter vessels and a broad band of cortical tissue and bark. This kind of organization is typical of plants that are irreversibly attached to surrounding vegetation by wide-angled branches. (C) Young climbing axis showing narrow pith, large proportion of dense stiff, juvenile wood and narrow band of external cortex. This kind of organization characterizes the stiffest stems of M. aff. quinquepartita, characteristic of vertical stems that are lightly attached to host supports via petiole bases.

Fig. 6.

(A) Transverse section (TS) of juvenile wood; (B) TS of lianoid wood; (C) TS of dense juvenile wood – note presence of abundant starch bodies; (D) TS of lianoid wood – note larger lumen size and thinner wall thickness of fibre tissue compared with the juvenile wood observed. Scale bars: (A, B) = 500 µm; (C, D) = 50 µm.