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In this issue of New Phytologist, Kitajima et al. (pp. 640–652) provide new insights into how leaves resist the rigours of life in the rainforest understory, seeking explanations of durability at multiple levels, and confirming the utility of a new way of standardizing toughness measurements. Their paper relates leaf structural and material properties, as well as chemical composition, to seedling leaf lifespan, herbivory and survival of 24 rainforest tree species in a common garden experiment in gap and understory environments.
‘Terms like “toughness” have been used rather loosely by plant biologists, in contrast with the specific terminology of engineering.’
Persistent leaves are common in a range of habitats where only low rates of net carbon gain and growth are possible, such as nutrient-poor soils, alpine and boreal ecosystems, and the shaded understories of rainforests. A range of structural and chemical properties of leaves have been interpreted as defences that prolong leaf lifespan by protecting against herbivores, pathogens and physical stresses (e.g. Choong, 1996; Coley & Barone, 1996; Read & Sanson, 2003; Onoda et al., 2011). The impressive correlations of leaf lifespan with leaf dry mass per area (LMA) in global datasets (Reich et al., 1999; Wright et al., 2004) might suggest that robust construction is what really counts. However, this straightforward interpretation seems at odds with the fact that shade leaves often live longer than sun leaves of the same species, despite their lower LMA (Lusk et al., 2008).
Terms like ‘toughness’ have been used rather loosely by plant biologists, in contrast with the specific terminology of engineering (Read & Sanson, 2003). Kitajima et al. instructively consider leaf toughness at three levels: per unit surface area (structural level), per unit volume (material level or tissue level) and per unit dry mass (mass level) (Fig. 1). Structural toughness is an indicator of a leaf’s overall resistance to external force (e.g. wind or falling debris), which can be increased by a thicker lamina and/or tougher material. Material toughness (also called ‘fracture toughness’ in engineering) can be increased by high tissue density and high specific toughness (called ‘density-corrected toughness’ in Kitajima et al.). Specific toughness was recently shown to be a major contributor to leaf structural toughness (Onoda et al., 2011); this is not surprising, as density measurements do not distinguish cell wall components from cell contents, which contribute between 14% and 77% of leaf dry mass (Onoda et al., 2011). Leaves with high specific toughness are unattractive to herbivores not only because more energy is required to ingest a given amount of biomass, but also because their large cell wall fraction reduces their nutritional value (Clissold et al., 2009; Lusk et al., 2010). Specific toughness of shade leaves was found to be higher than that of sun leaves of the same species, which might help explain the persistence of shade leaves despite their having smaller LMA than sun leaves (Onoda et al., 2008; Lusk et al., 2010).
Cellulose, not lignin, makes leaves tough
As far as we are aware, Kitajima et al. are the first authors to explicitly examine the contributions of different cell wall components to specific toughness of leaves. Their finding – that cellulose content is by far the best predictor of toughness – is a jolt to the vague notion that ‘lignification’ is what makes plant tissues ‘toughen up’. This finding may be news to many of us who focus on leaves, even though scientists studying wood have long known that cellulose, rather than lignin, is what gives wood fibres most of their strength (Winandy & Rowell, 1984). The lignin content of leaves is, however, known to strongly influence decomposition rates and hence nutrient cycling (Melillo et al., 1982). Although leaf toughness also impacts on decomposition rates (Cornelissen & Thompson, 1997), it thus transpires that the lifespans of leaves and their posthumous effects on ecosystem processes are differentially influenced by two of the main components of the cell wall.
What determines leaf lifespan?
Kitajima et al. use path analysis to show that all three levels of toughness influence lifespans of rainforest tree seedlings. They examined direct and indirect effects of cellulose content, lamina density and each level of toughness on leaf lifespan by comparing alternative path models. Two aspects are of particular interest. First, lamina thickness contributed much less to leaf lifespan than did tissue density, confirming a pattern reported in at least three recent studies in rainforests (Kitajima & Poorter, 2010; Lusk et al., 2010; Westbrook et al., 2011). Lamina density and lamina thickness are two components of LMA, a well-known correlate of leaf lifespan both within and across habitats (Reich et al., 1999; Wright et al., 2004). Second, lamina density contributed to leaf lifespan not only via material toughness (Fig. 1) but also directly (Fig. 2). Yet it remains uncertain exactly how lamina density itself contributes to leaf lifespan. High lamina density may result from limited intercellular airspaces or from a high dry matter content (DMC, dry mass/fresh mass) (Poorter et al., 2009). Field studies have repeatedly found that leaves with high DMC (less water content) are unattractive to herbivores (e.g. Coley, 1983), but it is not clear whether it is the high DMC per se that deters herbivores, or high material toughness and/or any other defence mechanisms via high DMC. Similarly, there is no obvious a priori hypothesis linking leaf lifespan to intercellular airspaces.
While it seems clear that leaf lifespans of juvenile trees in humid forests are related to tissue density rather than lamina thickness, this pattern might not be generalizable to other situations. In semi-arid sclerophyll vegetation, for example, leaf lifespan is strongly correlated with lamina thickness as well as lamina density (Wright & Westoby, 2002; Mediavilla et al., 2008). Since thicker laminas are often found in sunny or arid habitats (Onoda et al., 2011), quite different suites of traits may be selected for in these environments. Similarly, understory plants are sheltered from wind damage, which might reduce the importance of structural toughness (to which lamina thickness contributes; Fig. 1) relative to material or mass-level toughness, compared to plants growing in open environments. Furthermore it remains to be seen if the low respiration rates of the persistent leaves of shade-tolerant plants (Baltzer & Thomas, 2007) have parallels in other unproductive environments. Although this and other recent papers by Kitajima and colleagues have helped us understand the leaf traits favoured by natural selection in shaded understories, plant ecologists therefore still face some big challenges in developing an integrated global understanding of the determinants of leaf lifespan and associated traits.