In a given light microclimate, differences in light interception between alternative shoot architectures must result from differences in leaf orientation and self-shading. In the current study we quantified the effect of both leaf angle and self-shading on tuft-scale leaf display and light interception. We also assessed the consequences of nonlinear light-response curves for the photosynthetic benefit accruing from light interception. So, what was the relative influence of variation between species in leaf angle and self-shading? and which plant traits were they associated with?
The current study extends previous work on the ecological significance of leaf angle variation in single or few species simulation studies (Ezcurra et al., 1991; Ryel et al., 1993; Pearcy & Valladares, 1999; Valladares & Pugnaire, 1999; Werner et al., 2001b) to a large multispecies comparison. Supporting previous work, this study found that species with shallower-angled leaves intercepted substantially more light when the sun was at high angles in the sky (midday; summer; low latitudes), while species with steeper leaves intercepted a greater proportion of their daily PFD-budget from low angles in the sky (morning, afternoon; winter; high latitude).
As expected, species with shallower leaf angles had greater whole-day light interception than steeper-leafed species, except in winter. Our working hypothesis was that the diminishing returns on high PFD would qualitatively change this result for whole-day carbon gain, such that steeper-leafed species performed better overall. Consistent with this hypothesis, a proportion of leaves in steeper-leafed species did achieve higher light incomes (and hence carbon gain) at low light angles at each end of the day, together with sufficient light income for near-maximum carbon gain across the middle of the day (example in Fig. 5).
However, our hypothesis proved incorrect at the scale of whole tufts due to the strong influence of leaf azimuth on the projection of leaf area in steeper-leafed species (Fig. 2a–b). Species with steeper leaf angles had a substantial proportion of leaf area exposed to very low light intensities at all times (Fig. 5), dragging down total tuft carbon gain. Similar interspecific differences would emerge independent of the particular light response curve used (examples in Fig. 5), although quantitative differences might be greater under light-response curves having higher asymptotic photosynthetic capacity. In general, the results of this study therefore support the notion that steeper leaf angles function to reduce exposure to excess radiation during the middle of the day (Ehleringer & Werk, 1986; Ryel et al., 1993; King, 1997; Pearcy & Valladares, 1999; Valladares & Pugnaire, 1999; Werner et al., 1999; Werner, 2002), at the expense of potential daily carbon gain, more than to take photosynthetic advantage of low angle light. While this is not a new or controversial argument about steeper leaf angles, few data have previously been available to test the proposition across many species.
Costs associated with the higher light interception in shallow-angled species across the middle of the day include increased leaf temperature, higher risk of overheating, and higher risk of photoinhibition. Excess light interception increases leaf temperature. This may be a disadvantage, increasing respiration rates more than photosynthetic rates, and decreasing water use efficiency (King, 1997). Species with shallow leaf angles presumably face a greater risk of overheating when transpirational cooling is limited by water deficits.
Another cost of high light interception is the increased susceptibility to reversible (Martinez-Ferri et al., 2000) or irreversible photosystem damage (Werner et al., 1999). Mild photoinhibition in high light leaves, incorporated into simulations of an oak canopy (Werner et al., 2001a), decreased daily carbon gain by at least 8%. Irreversible photosystem damage in horizontal leaves during drought led to subsequent leaf abscission in a Mediterranean Cistus species (Werner et al., 1999).
Given the costs and benefits of different leaf angles, we might expect the leaf angle of species to be co-ordinated with the average habitat. Ehleringer (1988) and Smith et al. (1998) investigated the patterns in leaf angle across precipitation gradients in 159 and 209 species, respectively. Mean leaf angle became progressively steeper in both herbs and shrubs with increasing aridity. Similarly, within sites steeper leaf angles may be beneficial in high light environments, such as at the top of canopies or in more open habitats. Shallow leaf angles may be particularly advantageous in light limited understoreys (King, 1997).
Despite this, a wide range of leaf angles is still observed within a common light environment. Studies reporting a gradient in leaf angle through a canopy often note that there is a wide range of leaf angles at any given depth or light intensity (Niinemets, 1998; Werner et al., 2001b). Similarly in the present study steeper-leafed species were distributed throughout all light environments in the vegetation.
Self-shading within tufts
Variation in leaf angle explained only a small proportion of variation in instantaneous or whole-day potential carbon assimilation between species (Tables 1, 2). Up to 92% of variation was explained by the average level of self-shading within the tufts. Numerous studies have identified the importance of reducing self-shading for maximizing intraspecific carbon assimilation (Honda & Fisher, 1978; Pearcy & Yang, 1998), but little has been known about the levels of self-shading across species. Species studied here ranged from 13% to as much as 60% self-shading of projected leaf area within tufts (branching units). Similar levels of self-shading at the shoot level can be inferred from the low display efficiencies (0.1–0.2) of shoots of Norway Spruce (Stenberg et al., 1999). This level of shading is surprisingly high, recalling also that additional within-plant shading will result from the interaction between different shoots or tufts on the whole plant.
In the present study, smaller-leafed species suffered more self-shading, despite having less total leaf area per tuft, a smaller LAI within the tuft outline and less leaf area per meter stem. The higher self-shading was due both to crowding of leaves close to each other and to proximity of leaves to the stem. This is consistent with results from simulation studies manipulating virtual plants. Properties of smaller-leafed species, such as increased leaf-clumping (de Castro & Fetcher, 1999), decreased petiole length (Takenaka, 1994), decreased internode length (Niklas, 1988), and decreases in the relative distance of leaf area from the stem (Takenaka, 1994), have each been shown to reduce light capture and carbon gain considerably via effects on shading.
The most-discussed benefit of smaller leaves is the ability to shed heat rapidly by convection, so that small leaves do not warm above air temperature as much (Parkhurst & Loucks, 1972; Givnish & Vermeij, 1976). The higher levels of self-shading shown here would similarly benefit small leaves more in bright sun than in shade. In low light, high self-shading should be a distinct disadvantage (Givnish, 1988), favoring larger-leafed species. In the same vegetation as the present study, Bragg & Westoby (2002) found a mild tendency for larger-leafed species to occur in lower light environments within a given height class.
Correlations among architectural traits
Species differed in mean leaf angle from 24° to 74° across 38 species from two sites. Structural costs to leaf angle have been investigated by Niinemets (1998) but, to our knowledge, not across species. In the current study leaf angle was weakly related to SLA (leaf area/dry mass), with steeper-leafed species having more dry mass for a given leaf area. It seems unlikely that this association arises from structural costs. Support costs are likely to be higher for shallower-leafed species if anything, requiring both a rigid lamina and a strong petiole to hold the leaf perpendicular to gravitational forces.
Across sites towards increasing aridity, average leaf size (see Westoby et al., 2002 for references) and plant height (Fonseca et al., 2000) decrease, leaves become more cylindrical and thicker, and leaf angle increases (Ehleringer, 1988; Smith et al., 1998). The patterns among coexisting species within sites are less well documented. In the present study there were no strong correlations among the important ecological traits of MLA, potential height, and leaf size. This suggests that within a site, each trait may be associated with different aspects of species ecological strategies.