- Top of page
Leaf texture can vary considerably among species, and can be characteristic of vegetation types and vegetation strata. For example, heath may have ‘harder’ leaves than rainforest, and overstorey plants may have ‘harder’ leaves than understorey plants. ‘Sclerophylly’ means ‘hard-leaved’, though biologists also use terms such as ‘tough’, ‘stiff’ and ‘leathery’ to describe such leaves. The term was coined by Schimper (1903) to distinguish xeromorphic plants with leathery leaves from those exhibiting succulence or leaflessness. However, sclerophylly can be found in a range of environments and its functional significance is uncertain. Hypothesized roles include resistance to water deficits (Schimper, 1903; Oertli et al., 1990), resistance to, or a consequence of low-nutrient soils (Loveless, 1961; Beadle, 1966), enhancement of leaf longevity by leaf protection (Chabot & Hicks, 1982; Turner, 1994a) and as a nonspecific evolved response to, or consequence of, a wide range of environmental stresses (Salleo & Nardini, 2000). Leaf structure, including biomechanical properties such as toughness, may influence herbivory (Coley, 1983; Choong, 1996; Gutschick, 1999) and the community composition of herbivores, including their diversity and density (Peeters et al., 2000; Peeters, 2002), and potentially affects other trophic levels within the community (Press, 1999). Hence, leaf biomechanical properties may play a substantial role in structuring the organization of ecosystems.
Despite the apparent ecological significance of sclerophylly, there is still relatively little known about the mechanical properties that characterize scleromorphic leaves. Much of what is known about leaf mechanics is based on petioles rather than leaf laminae, because the latter are difficult to model analytically (Niklas, 1999). A better understanding of the mechanical components of leaf texture should assist in teasing apart their function, and hence improve our understanding of questions related to the adaptive significance of sclerophylly (Choong et al., 1992; Edwards et al., 2000). In particular, does sclerophylly (i.e. having hard, tough, leathery leaves) have a single function (and what is it?) or does it confer benefits across a range of environmental stresses? Is this function achieved by a single mechanical property or by a group of mechanical properties, each of which may have independent or interacting effects? Furthermore, is sclerophylly even of adaptive significance per se, or is it no more than the consequence of adaptive or nonadaptive anatomical and physiological features (e.g. Salleo & Nardini, 2000)?
In Fig. 1 we show how leaves may vary in three properties that may be related to sclerophylly: strength, toughness and stiffness. Several studies have examined the mechanical properties of a wide range of species in relation to sclerophylly or related issues (Choong et al., 1992; Turner et al., 1993; Edwards et al., 2000; Wright & Cannon, 2001; Wright & Westoby, 2002). These authors found that scleromorphic leaves (sclerophylls), as judged by leaf mass area (syn. specific leaf weight, specific leaf mass: leaf mass per unit area), or the Loveless sclerophylly index (percentage fibre per unit protein; Loveless, 1961), or a subjective categorization/index of sclerophylly based on leaf texture (Edwards et al., 2000), had high toughness (work to fracture) (Edwards et al., 2000; Wright & Westoby, 2002), specific toughness (toughness expressed per unit leaf thickness) (Choong et al., 1992; Turner et al., 1993; Edwards et al., 2000; Wright & Cannon, 2001) and high strength and/or specific strength (strength per unit leaf thickness) (Choong et al., 1992[measured as resistance to a penetrometer]; Edwards et al., 2000). In addition, Reich et al. (1991) showed that leaves with long lifespans, and low specific leaf area (inverse of leaf mass area) have high force to fracture (termed ‘toughness’ in that paper). These conclusions were drawn from fracture tests of tearing (Edwards et al., 2000), punching (Reich et al., 1991; Choong et al., 1992; Turner et al., 1993; Edwards et al., 2000) and shearing (Choong et al., 1992; Turner et al., 1993; Edwards et al., 2000; Wright & Cannon, 2001). All these studies included both soft and scleromorphic leaves (to varying degrees), but only Edwards et al. (2000) investigated a broad range of test types, and none included flexural tests. Choong et al. (1992) viewed toughness (named specific toughness by us to differentiate it from whole-leaf toughness which is influenced by leaf thickness, see Table 1) as the core attribute of a sclerophyll. However, in describing sclerophylls, botanists have used the terms ‘hard’, ‘tough’, ‘stiff’ and ‘leathery’ (Schimper, 1903; Grubb, 1986). These terms suggest that a range of properties may be important in producing the scleromorphic leaf, though each of these terms has been used in a general sense, without strict definition that allows measurement. Botanists have most often used indirect indices such as leaf mass area or the Loveless index to measure sclerophylly, rather than textural properties. We have argued that measurement of textural properties, as inherent in the term ‘sclerophylly’, will be more useful than indirect indices, and that defined and quantifiable properties as used by materials engineers will be most useful (Edwards et al., 2000). However, rather than assume that only toughness has any functional significance in sclerophylly, we address a broad range of properties that relate to terms used by botanists over the last 100 years.
Figure 1. Representations of force-displacement curves of four leaves with contrasting mechanical properties. Strength is defined as the maximum force to fracture per unit area over which the force is applied. Toughness is defined as the work to fracture, measured as the area under the force-displacement curve. Stiffness is related to the initial slope of the curve, or stress per unit strain. In this diagram, Plant A has the same toughness as Plant B, but is stiffer and stronger. Plant C is stiffer than Plants A and B, stronger than Plant B, but is not as tough as Plants A and B. Plant D is stiffer, stronger and tougher than all other plants. This diagram is simplified and does not show any alterations of slope associated with changes from elastic to plastic deformation.
Download figure to PowerPoint
Table 1. Measured and derived mechanical properties used in this study (modified after Jackson, 1992; Edwards et al., 2000; Sanson et al., 2001)
|Mechanical properties||Calculation||Property being measured|
|Punch strength||Fmax/A (N m−2)||Absolute punch strength of the whole leaf at the point of testing (influenced by leaf thickness).|
|Specific punch strength||(Fmax/A)/T (N m−2 m−1)||Punch strength per unit leaf thickness at the point of testing.|
|Work to punch||(F/A) × D (J m−2)||The absolute amount of work done to force the punch through the leaf (influenced by leaf thickness)|
|Specific work to punch||((F/A) × D)/T (J m−2 m−1)||Work to punch the leaf per unit leaf thickness.|
|Work to shear||(F × D)/W (J m−1)||The absolute amount of work done to shear the leaf per unit leaf width (influenced by leaf thickness).|
|Specific work to shear||((F × D)/W)/T# (J m−2)||Work to shear the leaf per unit leaf thickness.|
|Force to tear||Fmax/W||The force to tear the leaf per unit leaf width|
|(N m−1)||(influenced by leaf thickness).|
|Tensile strength||(Fmax/W)/T# (N m−2)||Strength to tear the leaf.|
|Work to tear||(F × D)/W (J m−1)||The absolute amount of work done to tear the leaf per unit leaf width (influenced by leaf thickness).|
|Specific work to tear||((F × D)/W)/T (J m−2)||Work to tear the leaf per unit leaf thickness.|
|Young modulus (E)||(F/D) × S3/(48 I) (N m−2)||Stiffness or elastic resistance to bending, corrected for effects of the dimensions of leaf material (where the second moment of area, I, = W T3/12).|
|Flexural stiffness (EIW)||(F/D) × S3/(48 W) (N m2 m−1)||Stiffness or elastic resistance to bending, corrected only for strip width.|
In this paper we describe properties from both fracture and flexure tests of ‘dicot’ species (eudicots and magnoliids) that comprise a wide range of leaf textures including highly scleromorphic leaves. In a previous study we investigated native Australian plants growing in close proximity (Edwards et al., 2000). Correlations among leaf characters may therefore have been strongly influenced by a common evolutionary history (both environment and phylogeny) of the study plants. In the present study we use 32 species, each from a different family to reduce phylogenetic bias, from across the world but grown in the same location (Royal Botanic Gardens, Melbourne, Australia). The major aim was to determine the mechanical properties of sclerophylls, including the best explanators of sclerophylly. That is, are sclerophylls well-characterized by a single mechanical property, or group of properties, or are there different ways of being perceived as sclerophyllous, i.e. can different combinations of mechanical properties produce sclerophylls? Mechanical properties were tested against one direct and two indirect indices of sclerophylly, and the associations between sclerophylly and leaf nitrogen, phosphorus and fibre concentrations were also measured.
- Top of page
Six major conclusions regarding the biomechanics of sclerophyllous leaves can be drawn from this study:
(1) Sclerophyllous leaves have high strength to punch, work to punch, work to shear, force to tear and EIW (all ‘structural’ properties), i.e. sclerophyllous leaves are generally stronger, tougher and stiffer than softer leaves. The same conclusion is reached irrespective of the sclerophylly index used (BSI, LMA and SI). High strength and high toughness are usually mutually exclusive in isotropic materials. However, there are ways of combining materials to give high strength and promote high toughness (Atkins, 1974; Atkins & Mai, 1985). For example, high toughness can be achieved in structures comprising strong materials by mechanisms that promote fibre pull-out (the use of strong fibres glued weakly to the adjacent matrix, allowing dissipation of the fracture energy as the fibre shears through the matrix), together with other features that arrest cracks once they have been initiated (Atkins & Mai, 1985). The known structure of leaves can achieve such combinations of properties (high strength, toughness and stiffness) by incorporating the high strength of cellulose in structures that act at various scales (cellulose microfibril to whole-leaf anatomy) to enhance toughness (e.g. cellulose chains or vascular strands provide fibre–pull-out and air spaces arrest cracks) and stiffness (e.g. positioning S1 and S2 layers at different angles in the cell wall).
(2) Sclerophyllous leaves on average increase more in toughness than strength, and in flexural stiffness more than strength or toughness. This stiffness could be conferred, for example, by thickening the cuticle or the outer wall of the epidermis. This thickening could provide a direct effect as well as an indirect effect of thickening the most distant tissues from the central axis of the leaf (increasing EI). Thickening the cuticle need not substantially increase the strength or toughness of the leaf.
(3) Sclerophyllous leaves, on average, have higher specific strength, specific toughness and E (‘material’ properties, i.e. standardized for leaf thickness). However, sclerophylly is better characterized by whole leaf (structural) properties than by material properties. In this study we have ignored some aspects of leaf structure that may contribute to whole leaf mechanics, because of our assumption that sclerophylly is best characterized by lamina properties rather than midrib and margin properties. However, whole-leaf properties can be influenced by both of the latter. For example, the midrib of some species, such as Banksia marginata, is a greater proportion of the width of the leaf, which would strongly influence whole-leaf flexural properties. The revolute margins of M. grandiflora, and undulating and reinforced margins of I. aquifolium, must also influence flexural properties in particular. However, estimation of whole leaf properties is particularly difficult in such leaves because of their extreme anisotropic nature and tissue arrangement.
(4) Punch test properties of intercostal lamina correlate similarly with the sclerophylly indices to the random punches across the leaf lamina. That is, sclerophyllous leaves generally have strong and tough intercostal tissue, irrespective of the properties and densities of secondary veins. Leaf anatomy will be discussed in a later paper.
(5) Hierarchical partitioning indicated that strength, toughness and flexural stiffness each made a substantial independent contribution to the variance in sclerophylly indices, but the best explanators were flexural stiffness and strength, with the best predictive model being a combination of these two properties. In the case of BSI, flexural stiffness contributed 1.7× that of toughness, and 1.2× that of strength. BSI is derived from ranks, rather than from values. Hence, the shape of the relationship of BSI with the mechanical variables may change if botanists had assigned relative values rather than only ranks. However, analyses in relation to the other two indices, LMA and SI, yielded the same conclusion as for BSI. Choong et al. (1992) considered that sclerophylly was a function of fracture toughness (syn. specific work to shear) rather than whole lamina properties that are influenced by leaf thickness. However, from our study there is no evidence that toughness per unit thickness is a superior explanator of sclerophylly; instead it correlated less well with sclerophylly indices than toughness uncorrected for leaf thickness. Furthermore, from the definitions of sclerophylly used in the past, it is not clear that specific work should be a more central property to leaves described as hard, stiff, tough, leathery (e.g. Schimper, 1903) than stiffness and strength. ‘Hardness’ as defined by materials engineers is a surface property that is appropriate to measure in isotropic materials, but which is less meaningful in relation to whole leaf properties, and when used by Schimper and others ‘hardness’ was probably not used in this sense (Edwards et al., 2000) and this usage might relate more to flexural stiffness. Lucas et al. (2000) note that hardness may be influenced by features such as local deposits of silica, and this feature probably warrants further investigation, even if not a major contributing factor to sclerophylly.
The apparent importance of flexural stiffness is consistent with the methods used by botanists to rank the leaves. When asked after ranking the leaves what properties influenced their decision, all botanists cited bending or flexibility as a major character, i.e. that sclerophyllous leaves were more difficult to bend. No one cited breaking or fracture as a major character. In the bending tests used, the bending is undertaken over a short displacement, and shearing stress is minimized, i.e. the test probably approximated quite closely what the botanists were attempting by hand. Cowling & Campbell (1983) used a subjective classification of sclerophylls as ‘leaves hard, coriaceous and thick, breaking when folded’. In the folding, they bent the leaves over a sufficient range to ensure their fracture, and therefore may have a slightly different sense of sclerophylly from the botanists ranking sclerophylly in this study, i.e. they emphasized the property of brittleness. Atkins & Mai (1985) distinguish between elastic, elastoplastic and plastic fracture essentially by the size of the region adjacent to the crack surface that is deformed plastically and hence irreversibly during the fracture process. In elastic materials this region is very small and so the two surfaces can be put back together almost perfectly. Such materials are defined as brittle, and elastic fracture is often called brittle fracture for this reason. Brittleness should not be confused with stiffness because some materials such as jelly can fracture in a brittle fashion. In our experience some stiff sclerophyllous leaves, such as those of Eucalyptus baxteri which have closely packed layers of turgid cells throughout the mesophyll, snap (often audibly), in a brittle fashion when folded beyond their yield strength. However, in others, such as Banksia marginata, the crack develops slowly with almost imperceptible noise as individual veins break. In these leaves the region around the crack is more damaged and the two surfaces do not fit perfectly. This is more characteristic of elastoplastic fracture (Atkins & Mai, 1985). The eucalypt cells have very high connectivity, and coupled with high turgidity there is little opportunity for them to plastically deform or slide over each other, with consequent brittle fracture. There is little opportunity for fibre pull-out in the cell walls promoting high irreversible work to fracture, and plastic work of deformation of surrounding tissues. Conversely, B. marginata fractures with extensive fibre pull-out and consequent high work to fracture and achieves high stiffness in different structural ways (Read et al., 2000). Therefore, the coriaceous leaves identified by Cowling & Campbell (1983), may be a subset of a larger group of scleromorphic leaves. Since sclerophylly has been so loosely defined, botanists may vary in their concept of the textural properties of sclerophylly and we do not claim that the botanists in our study were more ‘correct’ in their concept of sclerophylly than any others. Even so, hierarchical partitioning does indicate that EIW and strength are also the best explanators of sclerophylly as judged by the objective indices, LMA and SI, though these indices have their own deficiencies (Witkowski & Lamont, 1991; Groom & Lamont, 1999; Edwards et al., 2000).
(6) Leaves varied considerably in all the properties tested, and in the way they combined properties, both structural and material. However, while sclerophylls are generally stiff, strong, and tough, there is some variation in the ways of achieving sclerophylly. This has implications for ways in which studies of leaf form and function are undertaken. There has been a tendency to concentrate on specific toughness, or ‘toughness’ as measured by a penetrometer (usually measuring force to fracture). This has yielded some interesting patterns, such as in studies of herbivory and recent studies by Wright & Westoby (2002) on adaptive aspects of leaf form. There may be a priori reasons for targeting features such as toughness or specific toughness, but in their absence, studies of the adaptive significance of leaf texture may benefit from including more than one biomechanical property. For example, in studies of herbivory, strength is relevant in terms of the force required to bite a leaf, and toughness in terms of the energy of processing the leaf meal.
Sclerophylly correlated positively with fibre (NDF) concentration and negatively with nitrogen and phosphorus, consistent with other studies (e.g. Loveless, 1961; Sobrado & Medina, 1980; Medina et al., 1990; Specht & Rundel, 1990; Reich et al., 1991; Choong et al., 1992; Turner, 1994b; Read et al., 2000). Furthermore, the estimated protoplasmic concentrations of nitrogen and phosphorus correlated negatively with the sclerophylly indices, indicating that low mass-based estimates in sclerophyllous plants are more than just an effect of dilution by cell wall, although the relationships with sclerophylly were weakened when expressed as an estimated protoplasmic concentration. These results are significant in that all plants were growing under similar conditions of climate and soil, and hence these correlations probably represent inherent capacities of the plants rather than direct effects of the contrasting environments to which the plants are naturally restricted.
We again emphasize that species can achieve sclerophylly (in its textural sense) in different ways, both mechanically as seen in this study, and anatomically (Read et al., 2000). Furthermore, while structural properties (fracture strength, fracture toughness and flexural stiffness) are stronger correlates of sclerophylly than material properties, and strength and stiffness contribute most strongly to sclerophylly, this does not necessarily mean that these are the only, or even the most ecologically important, mechanical characteristics. It is likely that sclerophylly is a complex of associated mechanical characteristics with both overlapping and contrasting roles, and that the roles of individual properties will be difficult to tease apart for various reasons. Firstly, textural (mechanical) properties may have multiple functions or effects. Leaves must be mechanically designed to sustain static loads that leaf tissues impose on themselves and be able to twist and bend when subjected to larger forces such as wind (Niklas, 1999). Mechanical properties may influence resistance to water deficits (Schimper, 1903; Oertli et al., 1990) and tolerance of low-nutrient soils (Loveless, 1961), and may enhance leaf longevity by leaf protection (Chabot & Hicks, 1982; Turner, 1994a). Hence, the mechanical design of a leaf is likely to involve a compromise between the requirement to withstand static and dynamic loads (Niklas, 1999) as well as the requirement for design that enhances physiological performance under resource-poor conditions.
Secondly, the specific mechanical properties may act at different scales. For example, if sclerophylly provides an advantage by resistance to cell collapse due to negative turgor pressure (Oertli et al., 1990), then mechanical properties at the level of individual cells may be more relevant than properties conferred by arrangements of tissues. Even herbivores can be influenced by mechanical properties at different scales due to their different body sizes and characteristics of their mouthparts (Bernays & Hamai, 1987; Peeters, 2002). Salleo & Nardini (2000) suggested that sclerophylly may be a nonspecific evolutionary response to a range of environmental stresses, including those mentioned previously, as well as freezing and high light irradiance. This may be a direct evolutionary response, or an indirect response as in the leaf protection hypothesis, i.e. low resource availability favours sclerophylly because resource shortage selects for leaves with long lifespans (Chabot & Hicks, 1982; Turner, 1994a). If the former is true, then different mechanical patterns may be present in contrasting environments. If the latter is true, then similar mechanical patterns may be present under contrasting conditions of environmental stress. In our study we have investigated plants native to a wide range of environments; the results therefore represent ‘average’ trends that may mask different associations of mechanical properties in leaves adapted to contrasting environments. Whether the term ‘sclerophylly’ can be abandoned and replaced with more specific mechanical terms will be influenced by the outcomes of further studies, such as those comparing leaf mechanical properties in contrasting environments. For the moment we regard it as a useful term, so long as the above caveats are recognized.
It is tempting to assume that the mechanical pattern is adaptive. However, it is also possible that the key adaptive features are aspects of the anatomy that confer physiological benefit, such as a thick cuticle reducing water loss and heat gain, and that happen to confer certain mechanical properties, the latter not being adaptive but only by-products. In addition, the mechanical properties may arise from nonadaptive consequences of resource limitation (e.g. Salleo & Nardini, 2000). Hence, assessment of the functional and ecological roles of the mechanical properties of scleromorphic leaves will be difficult because of multiple roles of mechanical properties, the contrasting scales at which the properties exert their effects, and the potential difficulty of separating adaptive from nonadaptive roles.
Finally, why measure mechanical properties in studies of sclerophylly rather than a simpler property such as LMA (or the separate components of density and thickness) or SI? The limitations of SI as an index of sclerophylly have been noted previously (Witkowski & Lamont, 1991; Groom & Lamont, 1999). However, if plant resource allocation is the aspect of interest, then both LMA and SI may have more relevance than mechanical properties, though mechanical properties are relevant if benefits of resource allocation are considered in a broad sense. LMA (or SLA) has particular relevance to studies investigating allocation patterns in relation to photosynthetic performance and growth. SI may be particularly relevant to studies of palatability because it provides a measure of dilution of nutrients by cell wall. However, if the questions are centred on the potential function of the mechanical aspects of the leaf textural form, then LMA (and its components of density and thickness) and SI provide only a coarse estimate, since leaf mechanical properties are a function not just of quantity of material, or density, but also of the type of material and its arrangement. Measures of allocation such as LMA are valuable, together with measures of mechanical aspects of leaf texture, because they record different aspects of leaf form.