Journal of Experimental Botany, Vol. 51, No. 344, pp. 617-633,
March 2000
© 2000 Oxford University Press
Brittleness of twig bases in the genus Salix: fracture mechanics and ecological relevance
1 University of Freiburg, Institute of Biology II/Geobotanik, Schänzlestraße 1, D-79104 Freiburg, Germany
2 Harvard University, Herbaria, 22 Divinity Avenue, Cambridge, MA 02138, USA
3 CIRAD-Forêt, 73 rue J.-F. Breton, Bâtiment 16, BP 5035, F-34032 Montpellier, Cedex 1, France
4 University of Freiburg, Institute of Biology III, Schänzlestraße 1, D-79104 Freiburg, Germany
5 University of Freiburg, Botanic Garden, Schänzlestraße 1, D-79104 Freiburg, Germany
Received 26 March 1999; Accepted 25 October 1999
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Abstract |
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The twig bases within the genus Salix were investigated. Brittleness of twig bases as defined in the literature neither correlates with Young's modulus nor with growth strains, which were measured for S. alba, S. fragilis and S. xrubens. For the species S. alba, S. appendiculata, S. eleagnos, S. fragilis, S. purpurea, S. triandra, S. viminalis, and S.xrubens, fracture surfaces of broken twigs were investigated and semi-quantitatively described in terms of ‘relative roughness’ (ratio of rough area of fracture surface over whole area of fracture surface). The relative roughness clearly corresponds with the classification into brittle and non-brittle species given in the literature. An attempt was made to quantify brittleness with mechanical tests. The absolute values of stress and strain do not correlate with the brittleness of the twig bases as defined by the relative roughness. However, the ‘index stress’ (ratio of stress at yield over stress at fracture) or the ‘index strain’ (ratio of strain at yield over strain at fracture), correlate well with the relative roughness. The graphic analysis of index stress against index strain reveals a straight line on which the eight species are ordered according to their brittleness. Depending on growth form and habitat, brittle twig bases of willows may function ecologically as mechanical safety mechanisms and, additionally, as a propagation mechanism.
Key words: Growth strains, scanning electron microscopy, elasticity, fracture, plant ecology.
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Introduction |
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In the genus Salix, brittle twig bases are best known for the species S. fragilis, the Crack Willow. ‘A shoot bent back somewhat will snap cleanly away at the base: hence the name.’ (Mitchell and Wilkinson, 1985
). Other willow species also have brittle twig bases, however, they are said not to give the typical sound the Crack Willow gives when bent and broken. Shedding of twigs is described for several tree species (Millington and Chaney, 1973) as, for example, oaks (Chaney, 1979) and poplars (Dewitt and Reid, 1992; Höster et al., 1968). In these examples, the shedding is known as a natural self-pruning process. Twigs and small branches inside the crown, which have a negative net photosynthesis, can break off and thus increase the relative carbon gain of the tree. In the case of oaks, the twigs are dead or almost dead when they fall off. This is similar to leaves falling off in autumn. In both cases, the plants separate unnecessary material by an abscission layer. Abscission, in this case, is a physiological process including the differentiation of particular abscission layers and tissues (Dewitt and Reid, 1992). Nutrients and essential compounds will be resorbed and stored in the trunk, whereas toxic or otherwise ‘harmful’ metabolites will be stored in the leaves and twigs, respectively. This can be also considered as a plant excretion mechanism (Ford, 1986).
In contrast, willows and poplars shed living twigs. Like cuttings, these twigs can root and establish offspring (Galloway and Worrall, 1979; Beismann et al., 1997a). Populus develops a specialized abscission tissue and particular wood material is built around the twig base in the form of a collar (Höster et al., 1968). In the case of Salix, no abscission layer can be observed, except for those twigs that are shed in autumn after producing catkins in spring (von Höhnel, 1880). The brittle region at the twig bases of brittle willow species is anatomically not distinguishable under the light microscope. In both cases, with or without an abscission layer, an external mechanical force is needed to break off twigs and small branches. In most cases, wind forces can be responsible for the shedding of twigs, but also flooding and snow pressure may cause shedding. Although all species tested have to cope with mechanical loads, they are mechanically adapted in different ways according to their habitats. For example, failure due to bending loads occurs frequently in S. fragilis and S.xrubens at the twig bases whereas S. alba and S. appendiculata have more flexible twig bases (Beismann et al., 1997b). The different growth forms appear to be adaptive to specific habitat requirements.
These differences were tested to establish whether they correlated with mechanical properties measured in the elastic range, as was shown for other species (Brüchert et al., 1994; Wilmanns et al., 1985), or if they correlate with mechanical fracture (for a description of the mechanical parameters see Table 1). It is not difficult to characterize qualitatively a material as ‘brittle’ or ‘non-brittle’ by observing its behaviour when tested by hand, as seen by the traditional classification into brittle and non-brittle species found in the literature. However, it is more difficult to determine the brittleness of a material by rigorously testing its mechanical properties. In this study the correctness of the former classification was investigated by quantitative and reproducible mechanical tests.
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Breaking experiments were performed to determine the strain and the stress at fracture and at yield at the twig bases of eight different Salix species. In addition, the fracture surfaces of the eight Salix species were examined at the electron microscope level.
The aims of this investigation were (1) to describe biomechanical properties of the eight Salix species with respect to their brittleness at the twig base, (2) to explain the mechanism of failure by comparing fracture surfaces with mechanical properties, and (3) to deduce the ecological relevance for having brittle or non-brittle twig bases, in terms of growth form, habitat requirements, and the likelihood of twigs breaking.
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Species
Eight willow species were chosen for this investigation: Salix alba Linné, Salix appendiculata Villars, Salix eleagnos Scopoli, Salix fragilis Linné, Salix purpurea Linné, Salixxrubens Schrank (for reasons of simplicity the term species also includes the hybrid), Salix triandra Linné, and Salix viminalis Linné.
Four of the species have brittle twig bases and four have flexible twig bases (Lautenschlager and Lautenschlager-Fleury, 1994). In each group tree-like and shrub-like species occur (Table 2), although this classification is ambiguous, especially the growth form of S. appendiculata, which is neither shrub-like nor tree-like. All species were collected in SW Germany. Seven of the selected species grow on river banks or at the sides of creeks. A special case is S. appendiculata. This willow is mainly distributed in the European Alps, growing in so-called avalanche tracks, small valleys, often with creeks in them, which are the main ways for avalanches. Specimens of this species were collected in the Black Forest, at Mt Feldberg. Although the frequency of avalanches is smaller in comparison to the Alps, the plants are still exposed to heavy snow and avalanches. Salix triandra was collected close to St Peter in the Black Forest. It is distributed in floodplains and often grows within the area of maximum inundation. Salix eleagnos and S. viminalis were collected from the river banks of the Rhine. Salix eleagnos is distributed from the lowland to alpine valleys, whereas S. viminalis favours lower altitudes. Salix purpurea was collected from the riverside of the river Möhlin close to Hausen near Freiburg. It is a very common species, growing near riversides from colline to subalpine regions and is a typical pioneer on gravel sites. S. fragilis, S. alba and S.xrubens were also collected close to Freiburg. Salix fragilis grows in colline to montane floodplains, whereas S. alba favours the lowland floodplains. The hybrid between them, S.xrubens, grows in both habitats.
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Material for scanning electron microscopy (SEM)
Lateral twigs with diameters of 5–8 mm were broken off by hand. Twigs were broken in natural fresh condition having the cortex still attached and were air-dried before use. For each species, six twigs were broken. Both faces of the fractured samples were scanned, i.e. the fracture surface at the side of the main branch and the fracture surface of the lateral twig.
Scanning electron microscopy
The fracture surfaces of the broken twigs were examined using a scanning electron microscope (Cambridge Stereoscan 200, Leica, Bensheim, FRG). Air-dried specimens were fixed onto aluminium stubs with carbon paint and coated with a 25 nm thin gold layer in a sputter coater (Balzers SCD 040, Wiesbaden, FRG). Photographs of the complete surface and magnified details of either the tension or compression side of the fracture surface were taken.
The surface area with wood fibres torn out of fractured surfaces were determined with an electronic device built in the workshop of the Institute of Biology II/III, University of Freiburg. Only the tension side of the fracture surface of the bent twig was considered in this type of analysis. Dividing the area with torn out fibres by the total area of the tension side of the fracture surface gave a dimensionless number between 0 and 1, called ‘relative roughness’.
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Material for bending experiments
Twigs and branches of S. alba, S.xrubens, S. fragilis, and S. appendiculata were pruned after the vegetation period in autumn and tested in bending usually within 2 d after cutting but no longer than 4 d in storage. Between cutting and testing the twigs and branches were wrapped in wet cloth. The twigs were aged between one and nine years. Axes were inspected before testing to ensure that they were intact and macroscopically undamaged.
Bending experiments
Bending tests were carried out on a steel frame bending apparatus. Span distance and weight increments were varied according to the size and bending resistance of the material selected. Up to eight weights were applied manually and the maximum deflection for each weight increment was measured by observation with a dissection microscope. The twigs and branches were tested in 4-point and 3-point bending experiments (Speck, 1991; Vincent, 1992). Structural Young's moduli of the stems were calculated from the slope of the linear regression of the applied bending force versus maximum deflection.
The structural Young's modulus is a characteristic material parameter describing the mechanical bending properties of a plant stem independent of size and shape. The term ‘structural’ is used to emphasize that it represents an effective value of a heterogeneous composite material (Rowe and Speck, 1998; cf. Niklas, 1992, p. 209). It is calculated by dividing the experimentally determined flexural stiffness by the mean axial second moment of area of the tested stems. In order to minimize the influence of shear (Vincent, 1992), tests were carried out with a minimum span-to-depth ratio of 20. Previous tests and comparisons with the results of 4-point bending tests confirmed that the influence of shear is negligible when this ratio is 
20.
Material for growth strain measurements
Twigs of S. alba, S.xrubens and S. fragilis were cut with the main branch still attached. The lateral twigs had a diameter between 4 mm and 16 mm. To prevent an influence of the released stresses due to the end cuttings on the measurements, a distance of at least three times the twig diameter was left between the cuts and the study region.
Growth strain measurements
Longitudinal growth strains at the stem surface were measured by stresses released on the stem periphery, as described previously (Baillères et al., 1995, 1997). An extensiometric sensor (manufacturer HBM, type DD1) was used to measure the longitudinal growth strains at the stem surface. The total longitudinal growth strain was determined by the sensor after sawing two grooves with 5 mm distance to each side of it (Fig. 1). These cuttings were assumed to release locally existing stresses in the twigs. The observed strains are, therefore, proportional and have opposite signs to the real stresses in the twigs. The longitudinal growth strains were measured in microstrain (in µm m-1). The main branch was fixed in a clamp, leaving the lateral twig free. Two sensors were applied simultaneously on the upper (adaxial) and lower (abaxial) side of the lateral twig (the cortex was removed at the points of measurement). The sensors were attached as close as possible to the twig base. For each side of the twig base (adaxial and abaxial), 20 measurements were made. Missing values in Fig. 1A, B are due to experimental difficulties.
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Compression stress induces a swelling between the grooves; thus, the resulting longitudinal growth strain is positive. Tension stress induces a shrinkage between the grooves; thus, the resulting longitudinal growth strain is negative.
Material for breaking experiments
Twig junctions were cut off the trees and immediately put into plastic bags to prevent them from drying out. Lateral twigs had a diameter between 2 mm and 6 mm. Twigs of one, two and several years of age were distinguished. They were stored under moist and cool conditions (4 °C) for a maximum of 5 d before being examined, to ensure that the measured mechanical properties were the same as under natural conditions. Most samples were collected from individual trees to ensure genetically comparable samples. For S. viminalis and S. fragilis only, two trees for each sample set had to be chosen to get enough material. The number of samples per species was for S. alba=57, S. appendiculata=35, S. eleagnos=61, S. fragilis=82, S. purpurea=62, S. triandra=68, S. viminalis=54, and S.xrubens=70.
Breaking experiments
Mechanical tests were carried out on the twig junctions using an Instron universal testing machine (Instron Wolpert GmbH, Ludwigshafen, FRG, model 4466) with a computer interface capable of simultaneously recording applied force (F) and deflection ( f). To fasten the samples, the main branch, with a length of about 5 cm, was clamped over its entire length to leave the lateral twig free. The lateral twig was put into a ring-shaped clamp at a distance of about 1 cm from the junction into the main branch. The ring-shaped clamp was then connected to the tensile device of the Instron machine via a long steel stick. The compliance of this experimental set-up together with the compliance of the Instron machine was found to be negligible.
The lateral twig was pulled in a direction parallel to the length of the main branch to accord with the natural loading condition (Fig. 2).
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The following formulas for calculating stress and strain were used (for a derivation of the formulas see Young, 1989
): From the force applied at breakage, the bending moment was calculated using the lever arm (a). This is the effective lever arm at the moment of breakage. Using the bending moment (BM), the stress at fracture was calculated. The formula for cantilever bending was used to calculate the strain at fracture on the surface of the bent twig and corrected according to the angle (
) that occurred just before breaking (Fig. 2A).
Stress at fracture (
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The bending moment (BM) was calculated as follows:
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Strain at fracture (
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is the angle just before breakage.
Since the mathematical description of non-linear behaviour is not solved satisfactorily yet, the use of formulas developed for linear relationships, i.e. the behaviour within the elastic range, can only be an approximation. Since the calculation of stress and strain is not critically influenced by this problem, stress and strain should give realistic numbers to compare different species. Although the requirement of a homogeneous material is not fulfilled for the use of the formula for stress, it can be used as a good approximation for a comparison between the tested species, since the eight species do not vary significantly concerning their proportions of cortex, wood and pith. It is further assumed that in the bent stems the cross-sectional areas remain plane. An additional requirement for the formulas to be correct, is that the neutral axis in bending lies in the centre of the cross-section. This is fulfilled in good approximation, as can be seen from the SEM photographs (Figs 3–10). The change from tension to compression side, representing the neutral plane, is clearly visible and lies in the centre of the cross-section (marked with dots). The assumption of a central position of the neutral plane is also supported by the measurements of growth strains at the surface of twig bases. Growth strains differ only very slightly for the two sides of the twig bases.
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Stress and strain at yield
Stress and strain at yield were calculated with the same formulas, where Fcrit is the force applied at yield, f the deflection of the lateral twig at yield and the angle at yield (Fig. 2A).
Indices for stress and strain
The numbers for stress and strain at yield were divided by the numbers for stress and strain at fracture, resulting in a dimensionless number referred to as ‘index stress’ and ‘index strain’ respectively.
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Statistical tests
For the statistical analysis of the breaking experiments one-way ANOVA (analyses of variance) using the Scheffé's test were done with a significance level P<0.05.
The age of the twigs had no influence on the breaking properties, therefore twigs were grouped in one size class.
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Results |
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Analysis of the SEM pictures
The fractured surfaces of twigs showed marked differences among the species examined. Species with brittle twig bases generally show a smooth fracture surface, whereas non-brittle species have a rough fracture surface. In general, the fracture surface of a twig broken by bending shows two main areas. A tension side, on the abaxial surface of the bent twig and a compression side, on the adaxial part of the bent twig. Wood destroyed under compression usually shows a rough and crumbled structure, whereas breakage under tension produces smooth areas and areas with torn out fibres (Sell and Zimmermann, 1993a
, b). Therefore, in this study only the tension side of the broken twigs was considered. Figures 3–10 show: (A) an overview of the fracture surface of all tested species, (B) magnifications of the tension side, (C) magnifications of the compression side, (D) structures of special interest in higher magnifications for some of the species. The tensile fracture surfaces of the species S.xrubens and S. fragilis are very smooth (Figs 3A, 4A). In addition, there is nearly no height difference between the tension and the compression side of the broken twig. The amount of fibres torn out at the tension side of the fracture surface is very small. The smooth areas of the tension side give the impression that they were cut with a razor blade (Figs 3B, 4B). S. triandra, S. alba and S. viminalis have partly smooth surface areas but also have a considerable amount of areas where fibres are torn out at the tension side of the fracture surface (A and B on Figs 5, 6, 7). In contrast, S. purpurea and S. eleagnos generally had a very distinct height difference between the tension and compression sides (Figs 8A, 9A). In addition, it is sometimes not possible to break off a twig without damaging the main branch to which it was attached (Fig. 8D). In S. appendiculata, the main branch was injured severely in half of the breaking tests, or the wood material was squeezed together (Fig. 10A). In addition, a smooth surface could never be found on the tension side (Fig. 10B).
A conspicuous phenomenon is the occurrence of torn out fibres, which seem to cover bigger areas on the tension side of the fracture surface of those species which do not break easily at their twig bases (Figs 6B, 9B, 10B). The torn out fibres consist only of a part of the inner cell wall. This can be clearly seen in Fig. 6D. In the surrounding cells, the crack runs directly through the cell walls, breaking through the different layers of the cell wall. But the propagation of a crack can be stopped between layers. The microfibrils of the S2 layer are orientated in a very small angle against the longitudinal axis of the cell, whereas the S1 layer has an almost perpendicular orientation of microfibrils against the longitudinal axis of the cell. Figures 6D and 7D clearly demonstrate an orientation of fibrils nearly parallel to the longitudinal axis of the cell in the inner part of the cell wall where the S2 layer is visible as torn out fibres.
Relative roughness
Tree-like and shrub-like willow species are indistinguishable concerning their wood anatomy (Schweingruber, 1990). Also the three-dimensional structure of regions with torn out fibres is similar in all species and specimens. The height and diameter of torn out fibres are comparable in all observed cases. Thus, the amount of ‘rough’ regions on the tension side of wood on the fracture surfaces is probably proportional to the energy needed to create the fracture surface.
The proportion of rough regions per tension side of the wood, represented by the relative roughness, is highest for S. appendiculata and lowest for S.xrubens (Table 3). Clearly distinguished are four groups: S.xrubens and S. fragilis with the lowest values (less than 10% rough areas), whereas in S. triandra, S. alba and S. viminalis about 1/3 of the tension side shows torn out fibres. Half of the measured fracture surface is rough on the tension side in the cases of S. eleagnos and S. purpurea, and in S. appendiculata, finally, nearly the entire area of the tension side can be considered as rough (Table 3).
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Young's modulus of entire axes
The structural Young's modulus shows a distinct increase with the axial second moment of area that, in turn, correlates with the diameter of a stem, for S. alba, S.xrubens and S. fragilis, a pattern that is typical for self-supporting shrubs and trees (Speck, 1994; Rowe and Speck, 1998) (Table 4). Only in S. appendiculata is this tendency less pronounced, the structural Young's modulus varies randomly for all measured diameters between 1000 and 4000 MPa. The Young's modulus and its variation during ontogeny show no significant differences between brittle and non-brittle species. The age of the twigs had no effect on the Young's modulus.
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Growth strains
The values of growth strains, measured in microstrain, are shown in Fig. 11A, B on the adaxial and abaxial side of the twig base. The values are not corrected for the effects due to the twig acting as a cantilever. Growth strains at the twigs themselves show similar values compared to those at the twig bases and also increase in absolute values with increasing diameter (data not shown).
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All three species studied show comparable growth strains for similar stem sizes (Kruskal–Wallis One Way ANOVA on Ranks, P=0.165). The negative growth strains at the twig surface increase with increasing size of the twigs. Small twigs show growth strains close to zero.
Growth strains of the abaxial side of the twig base show positive values for the smallest twigs with diameters of 4–6 mm. These are of the order of strains induced by the twigs own weight. On the adaxial side of the twig bases the values are negative also for the smallest axes. However, the values found for the smallest axes below 6 mm are of the order of the strains effected by the twigs' own weight.
Growth strains at the abaxial side at the twig base show slightly more negative values for bigger axes (diameter >6 mm) compared to the adaxial side. This difference is significant (paired t-test, P=0.0002, pooled for all tested species).
Breaking experiments
Description of the breakage:
In this kind of experiment, breakage among the brittle species usually occurs at a distance of about 1–3 mm from the junction of the lateral twig with the main branch. The failure happens suddenly, often with an audible cracking sound. The fracture surface is on the tension side smooth or with few irregularities and almost perpendicular to the longitudinal axis of the lateral twig. The compression side can also be very smooth, but more often shows a rough surface. The load-deflection curve shows an abrupt decrease from the maximum load to almost zero. The linear part of the load-deflection curve is longer in comparison to the non-linear part. In some tests, breakage occurs within the linear part (Figs 2B, 12A).
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For the non-brittle species, breakage often occurs directly at the junction of the lateral twig with the main branch. The fracture surface is not perpendicular to the longitudinal axis of the lateral twig, but more or less parallel to the main branch axis. Frequently a failure running into the main branch occurs. While pulling at the lateral twig, parts of the main branch will be injured since wood fibres are torn out of it. The failure consists of a series of partial prefailure events (cf. Spatz et al., 1997
). The load-deflection curve shows a gradual decrease from the maximum load, with several small prefailure events. The linear part of the load-deflection curve is smaller in comparison to the non-linear part (Figs 2B, 12B).
Stress and strain at fracture:
For each species the mean values of the tested specimens are given with standard errors (Fig. 13A, B). Four species, S.xrubens, S. fragilis, S. triandra, and S. appendiculata, show relatively small stresses at fracture (between 17.7 and 28.4 MPa) (Fig. 13A). S.xrubens, S. fragilis and S. triandra are significantly different from the other four species, whereas S. appendiculata is not significantly different from S. eleagnos, but not from the other three. Stresses at fracture of the other four species (S. eleagnos, S. alba, S. purpurea, S. viminalis) are almost twice as high.
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S.xrubens (mean and SE, 5.6±0.3%) and S. fragilis (5.8±0.4%) have the lowest mean strain values at fracture (Fig. 13B). They are significantly different from the mean values of S. eleagnos, S. purpurea and S. appendiculata. Relatively high strain values are found in S. purpurea (10.2±0.4%) and S. eleagnos (10.7±0.5%). The mean values of strain at fracture for these species are significantly different from S.xrubens, S. fragilis, S. triandra, S. viminalis, and S. alba.
Stress and strain at yield
Stress at yield is highest for S. viminalis (19.3±0.9 MPa) and lowest for S. appendiculata (8.9±0.6 MPa) (Fig. 14A). The two species with the highest stress at yield (S. viminalis, S. purpurea) are significantly different from S. triandra, S.xrubens, S. eleagnos, and S. appendiculata. S. appendiculata is significantly different from S. fragilis, S. alba, S. purpurea, and S. viminalis.
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Strain at yield is highest for S. eleagnos (3.7±0.3%) and S.xrubens (3.6±0.2%) (Fig. 14B). Both are significantly different from S. viminalis, which has the lowest value for strain at yield (2.4±0.2%).
Relationship between biomechanical data and data from fracture surfaces
Regression analyses between stress or strain at fracture with relative roughness resulted in coefficients of determination of R2 smaller than 0.4. The same holds true for regressions between stress or strain at yield and Young's modulus for stems of comparable diameters with the relative roughness. When calculating the index stress (stress at yield/stress at fracture) and the index strain (strain at yield/strain at fracture) a dimensionless number between 0 and 1 results. These indices characterize the relationship between linear elastic behaviour and non-linear behaviour of the material. They are plotted against the relative roughness (Fig. 15A, B). Using a power function the regression model fits well with R2=0.79 (n=8) for index stress and R2=0.77 (n=8) for index strain against relative roughness. Plotting the index stress against the index strain a linear regression with y=1.18x-0.06 (R2=0.89) was calculated. Species are found to be arranged along this regression curve according to their brittleness at the twig bases, starting with the less brittle ones in the lower left corner to the very brittle ones in the upper right corner of the bivariate plot (Fig. 16).
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General description of the phenomenon
Failure of lateral twigs of a brittle species results in a smooth fracture surface, which is roughly perpendicular to the longitudinal axis of the lateral twig, i.e. the smallest possible injured area, where fungi and bacteria can infect the plant. Additionally, the wound is some millimetres distant from the main branch. The relict of the lateral twig can dry up and thus prevent the main branch from infection. This seems to be particularly important for Salix species, since this genus is known for its low content of tannic acid, which protects other woody plants against infection (Huber, 1961
). Failure of non-brittle species often does not only result in a bigger injured area, but also frequently damages the main branch severely and thus increases the danger of an infection. Considering the situation in natural environments, under windload or during flooding, most twigs will turn and bend in the apical direction, i.e. in the direction parallel to the mechanical load. Even snow will bend the smaller twigs mainly in this direction, since these twigs are more or less hanging down from the trees. The smaller danger of infections might be the reason why all species show a higher probability to break when loaded mechanically in the direction parallel to stem length towards the apex. This is not the case when loaded in the distal direction. In this case, more often the main branch is injured (data not shown). These considerations show that breaking in other than the apical direction is ecologically of minor importance. The distinction between brittle and non-brittle species given in the literature seems, therefore, not to be based on the possibility to break or not to break, but seems to depend more on how a twig breaks.
Biomechanical properties
Biomechanical properties, like Young's modulus, stress and strain at fracture or stress and strain at yield, do not match with the classification of brittle or non-brittle. The yield strain at the twig base is extremely high (c. 3%) in comparison to values found earlier in green stems (c. 0.3%) (Wessolly and Erb, 1998). This is very probably due to the fact that they measured wood samples from big stems which may have smaller strain values at yield than very young and undamaged twigs as tested in this study. No correlation with the brittleness could be found for the growth strains. Anatomical studies of tension wood in S. alba and S. fragilis show no difference in the composition and distribution between these two species, and no variation as to the location within a given species. This is consistent with the similar longitudinal growth strains found in S. alba and S. fragilis. The striking increase of growth strains with stem diameters confirms that prestresses in wood are built up during development and differentiation of wood fibres and tracheids (Baillères, 1997, 1995). The negative values for bigger twigs are comparable to values found in other tree species (Fournier-Djimbi et al., 1997). The very small but significant difference between growth strains at the adaxial and abaxial side of twig bases leads us to conclude that fibres are not arranged symmetrically in this region. This can be a reason for the slightly more negative growth strain values at the abaxial side.
Prestresses in wood are known to help resist stem breakage caused by bending loads (Archer, 1986; Fournier-Djimbi et al., 1997). It has been reported that the stems of tree species with a small growth strain to strain at yield ratio are less prone to fail by stem breakage than plants with a higher ratio (Wessolly and Erb, 1998). The three Salix species for which growth strains were determined, show a different breaking behaviour at the twig bases (Beismann et al., 1997a, b). Salix fragilis and S.xrubens are very brittle at their twig bases, whereas S. alba is more flexible. However, Salix alba, S.xrubens and S. fragilis show similar growth strains at their twig bases and also that the yield strain is not significantly different between the tested species in axes of comparable diameters. These results indicate that, in contrast to big stems (Wessolly and Erb, 1998), the ratio of growth strain over strain at yield can not be used to distinguish between brittle and non-brittle species for small twigs of Salix.
However, the classification into brittle or non-brittle species relates closely to the shape of the load-deflection curve (Fig. 12). A combination of the biomechanical properties represented by either the index stress or the index strain, respectively, correlated well with the relative roughness, which also correlates well with the classification into brittle and non-brittle (Fig. 15). When combining index stress and index strain in one plot (Fig. 16) the species are arranged along a straight line according to their brittleness.
Explanation of the failure mechanism
Brittleness of twig bases in the genus Salix correlates with the relationship between stress and strain at yield and at fracture. The total energy required to propagate a crack is the sum of the surface energy and the energy needed to produce plastic deformation (Niklas, 1992). If the range of non-linear behaviour is negligible, little energy is needed to propagate a crack. This means, almost only surface energy was required to propagate a crack. If the range of non-linear behaviour dominates the force-deflection curve (Fig. 12) more energy is needed to propagate a crack, which results in a rough fracture surface with torn out fibres. In less brittle to non-brittle species, the amount of torn out fibres increases gradually. The more fibres are torn out, the more friction between the cell wall layers has to be overcome, most probably between the S1 and the S2 layer, which are sheared against each other during the tearing process. This can be considered as a toughening mechanism for composite materials. To understand this mechanism completely a detailed investigation of the different compounds connecting S1 and S2 layer would be necessary. Also the orientation of fibres in the different cell wall layers should be known. Small angle X-ray scattering experiments are under way.
Ecological relevance of brittleness
For S. fragilis and for S.xrubens, the common hybrid between S. alba and S. fragilis, the index of stress and the index of strain are biggest of all the Salix species tested. In addition, both species have the smoothest fracture surfaces. These results indicate that in S. fragilis and S.xrubens the smallest energy requirement to break off a twig is found for all tested species. This enables S. fragilis and S.xrubens to propagate vegetatively via broken twigs. Vegetative propagation downstream could be confirmed for S. fragilis (Beismann et al., 1997a).
The two species S. triandra and S. viminalis are also known as brittle species and are found in Fig. 16 between S. fragilis and S. purpurea. This indicates that brittleness decreases gradually. Both (S. triandra and S. viminalis) are shrub-like and grow at riversides. They seem to occupy a similar ecological niche at different altitudes. S. triandra favours higher altitudes, whereas S. viminalis grows more frequently in lower altitudes. Both species can become submerged completely during flooding. The breaking ability is comparable and both species have a good ability to root from broken off twigs (H Beismann, unpublished data). Also in this case the brittleness at the twig bases can provide an additional propagation mechanism. However, considering their growth form, the brittle twig bases can also function as preformed breaking regions that allow the loss of a certain amount of twigs to reduce the pressure during inundation, and thus prevent the entire plant from stem breakage.
Such a safety mechanism (‘mechanical fuse’ in Usherwood et al., 1997) seems not to be of importance for the two species S. eleagnos and S. purpurea. Both are shrub-like and grow at riversides. They cluster in Fig. 16 below the brittle species. Although they can grow in similar habitats as the above-mentioned S. triandra and S. viminalis, they mainly grow as pioneers on gravel sites. S. eleagnos grows mainly in sub-alpine to alpine regions. The drop of the rivers is sharper and thus also the velocity of the water current. It is conceivable that the existence of brittle twig bases would result in too large a loss of biomass during inundation with high current speeds and additional gravel movements. The same holds true for S. purpurea, which frequently grows on gravel banks close to the water. Additionally, the establishment via broken twigs in a new habitat depends on the deposition site. Since gravel sites are flooded and, on more elevated sites the competition with other plants (e.g. S. alba) is high, brittle twig bases may not provide an efficient propagation mechanism. The evolution of very flexible twigs and twig bases, therefore, seems to be a functional adaptation in such habitats.
Although the tree-like S. alba can shed twigs, like all other Salix species tested, this does not seem to be a special adaptation to propagate vegetatively or to prevent stem breakage. S. alba clusters close to S. appendiculata and below all the other species in Fig. 16. In the natural extensive floodplains of the lowlands, high velocities of water current do not occur. During seed fall enough moist sand sites probably exist to ensure efficient generative propagation.
For S. appendiculata, which has its main distribution in the Alps, snow creeping is the main mechanical load. In addition, they have to sustain avalanches. In S. appendiculata even branches of a diameter up to several centimetres can be bent down and can be buried under heavy snow loads during winter. For survival under these conditions, it may be more important to withstand high strains than to withstand sudden gusts or turbulent flooding regimes. Salix appendiculata seems therefore to be more adapted to slowly creeping snow loads, causing high strains, but no sudden impacts.
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Conclusions |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionConclusionsReferences |
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Brittleness of twig bases seems to be an adaptation to mechanical loads, where it can function as a safety mechanism (‘mechanical fuse’ in Usherwood et al., 1997
) reducing the probability of dangerous infection or stem breakage by allowing twigs to be lost. For some species (S.xrubens, S. fragilis) it also seems to be an adaptation to provide an additional reproduction mechanism, due to the transportation and subsequent establishment of the broken off twigs in new habitats.
The parameter described as ‘relative roughness’ mirrors best the classification of brittle and non-brittle willow species given in the literature. The correlations between stress and strain at fracture and at yield, respectively, with the relative roughness are very poor. Also, the ratio of growth strains to strain at yield as proposed previously (Wessolly and Erb, 1998) reveals no significant correlation with the brittleness at twig bases. Neither of these biomechanical parameters alone reflects the brittleness of twig bases in Salix species or the relative roughness. However, a combination of stress at fracture and at yield or strain at fracture and at yield can be used. The correlation of these indices with the relative roughness is very high.
These results indicate that the relevant variable to distinguish a material as brittle or non-brittle is the relationship between linear-elastic and non-linear behaviour of a material.
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Acknowledgments |
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We wish to thank W Barthlott and C Neinhuis (Botanic Institute of the University of Bonn) for putting the scanning electron microscope at our disposal. We are also grateful to M Güthler for his kind help with the breaking experiments during his practical work in our laboratory. We thank G Calchera for his help and advice on measuring longitudinal growth strains. The work of H Beismann in the laboratory of CIRAD-Forêt in Montpellier was funded by a Franco-German PROCOPE project awarded to T Speck and NP Rowe which is gratefully acknowledged. We also wish to thank K Niklas and an unknown reviewer for their valuable and helpful suggestions on the manuscript.
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Notes |
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6 Present address and to whom correspondence should be sent. University of Basel, Botanic Institute, Schoenbeinstrasse 6, CH-4056 Basel, Switzerland. Fax: +41 612672980. E-mail:beismann{at}gmx.de
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References |
|---|
|
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|---|
Archer ST.1986. Growth stresses and strains in trees. Berlin: Springer-Verlag.
Baillères H, Chanson B, Fournier M, Tollier MT, Monties B.1995. Structure, composition chimique et retraits de maturation du bois chez les clones d’Eucalyptus. Annales Scientia Forestiere 52, 157–172.
Baillères H, Castan M, Monties B, Pollet B, Lapierre C.1997. Lignin structure in Buxus sempervirens reaction wood. Phytochemistry 44/1, 35–39.
Beismann H, Barker JHA, Karp A, Speck T.1997a. AFLP analysis sheds light on distribution of two Salix species and their hybrid along a natural gradient. Molecular Ecology 6, 989–993.
Beismann H, Speck T, Bogenrieder A.1997b. The wind in the willows, dispersal mechanisms and distribution of Salix alba, S. fragilis and their hybrid S.xrubens. In: Jeronomidis G, Vincent JFV, eds. Plant biomechanics 1997. Conference Proceedings I. Reading: Centre for Biomimetics at the University of Reading, 57–64.
Brüchert F, Bogenrieder A, Speck T.1994. Anatomischer und biomechanischer Vergleich der Sprossachsen von Alnus viridis (Chaix.) DC aus dem Schwarzwald und den Lechtaler Alpen mit Stockausschlägen von Alnus glutinosa (L.) Gaertn. aus dem Schwarzwald im Hinblick auf die Standortsökologie beider Arten. Berichte der Naturforschenden Gesellschaft Freiburg im Breisgau 82/83, 19–45.
Chaney WR.1979. Leaf and twig abscission relationships in a mature white oak. Canadian Journal of Botany 9, 345–348.
Dewitt L, Reid DM.1992. Branch abscission in balsam poplar (Populus balsamifera): characterisation of the phenomenon and the influence of wind. International Journal of Plant Science 153, 556–564.
Ford BJ.1986. Even plants excrete. Nature 323, 763.[Medline]
Fournier-Djimbi M, Sassus F, Combus J.G, Grzeskowiak V.1997. Growth strains and reaction wood. In: Jeronomidis G, Vincent JFV, eds. Plant biomechanics 1997. Conference Proceedings I. Reading: Centre for Biomimetics at the University of Reading, 231–236.
Galloway G, Worrall J.1979. Cladoptosis: a reproductive strategy in black cottonwood? Canadian Journal of Forestry Research 9, 122–125.
Höster HR, Liese W, Böttcher P.1968. Untersuchungen zur Morphologie und Histologie der Zweigabwürfe von Populus ‘Robusta’. Forstwissenschaftliches Centralblatt 87, 356–368.
Huber B.1961. Grundzüge der Pflanzenanatomie. Versuch einer zeitgemäßen Neudarstellung. Berlin: Springer Verlag.
Lautenschlager E, Lautenschlager-Fleury D.1994. Die Weiden von Mittel- und Nordeuropa. Bestimmungsschlüssel und Artbeschreibung für die Gattung Salix L. Basel: Birkhäuser Verlag.
Millington WF, Chaney WR.1973. Shedding of shots and branches. In: Kozlowski TT, ed. Shedding of plant parts. New York: Academic Press, 149–204.
Mitchell A, Wilkinson J.1985. A handguide to the trees of Britain and Northern Europe. London: Treasure Press.
Niklas KJ.1992. Plant biomechanics. an engineering approach to plant form and function. Chicago & London: The University of Chicago Press.
Schweingruber FH.1990. Mikroskopische Holzanatomie. Anatomie microscopique du bois. Microscopic wood anatomy. Birmensdorf: Eidgenössische Forschungsanstalt für Wald, Schnee und Landschaft.
Sell J, Zimmermann T.1993a. Das Gefüge der Zellwandschicht S2. Untersuchungen mit dem Feldemissions-Rasterelektronenmikroskop an Querbruchflächen von Fichten- und Tannenholz. Eidgenössische Materialprüfungs- und Forschungsanstalt. EMPA. Forschungs- und Arbeitsbericht Abteilung 115 Holz, Bericht 115/28, 1–27.
Sell J, Zimmermann T.1993b. Radial fibril agglomerations of the S2 on transverse-fracture surfaces of tracheids of tension-loaded spruce and white fir. Holz als Roh- und Werkstoff 51, 384.
Spatz H-Ch, Beismann H, Brüchert F, Emanns A, Speck Th.1997. Biomechanics of the giant reed Arundo donax. Philosophical Transactions of the Royal Society of London, Series B 352, 1–10.
Speck T.1991. Changes of the bending mechanics of lianas and self supporting taxa during ontogeny. Proceedings of the Second International Symposium SFB 230. Mitteilungen des SFB 230, Heft 6, 89–95.
Speck T.1994. Bending stability of plant stems: ontogenetical, ecological, and phylogenetical aspects. Biomimetics 2/2, 109–128.
Rowe NP, Speck T.1998. Biomechanics of plant growth forms: the trouble with fossil plants. Review of Palaeobotany and Palynology 102, 43–62.
Usherwood JR, Ennos AR, Ball DJ.1997. Mechanical and anatomical adaptations in terrestrial and aquatic buttercups to their respective environments. Journal of Experimental Botany 48, 1469–1475.
Vincent JFV. 1992. Plants. In: Vincent JFV, ed. Biomechanics—material, a pratical approach. Oxford: IRL Press at Oxford University Press 165–191.
von Höhnel FR.1880. Weitere Untersuchungen über den Ablösevorgang von verholzten Zweigen. Mitteilungen des forstlichen Versuchswesens Österreich 2, 247–256.
Wessolly L, Erb M.1998. Handbuch der Baumstatik und Baumkontrolle. Berlin: Patzer Verlag.
Wilmanns O, Bogenrieder A, Nakamura Y.1985. Vergleichende Studien des Pinus-Krummholzes in den Japanischen und europäischen Alpen. Tuexenia 5, 335–358.
Young WC.1989. Roark's formulas for stress and strain. New York: McGraw-Hill Book Company.
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