Optimal photosynthetic use of light by tropical tree crowns achieved by adjustment of individual leaf angles and nitrogen content

Abstract

Background and aims: Theory for optimal allocation of foliar nitrogen (ONA) predicts that both nitrogen concentration and photosynthetic capacity will scale linearly with gradients of insolation within plant canopies. ONA is expected to allow plants to efficiently use both light and nitrogen. However, empirical data generally do not exhibit perfect ONA, and light-use optimization per se is little explored. The aim was to examine to what degree partitioning of nitrogen or light is optimized in the crowns of three tropical canopy tree species.

Methods: Instantaneous photosynthetic photon flux density (PPFD) incident on the adaxial surface of individual leaves was measured along vertical PPFD gradients in tree canopies at a frequency of 0.5 Hz over 9-17 d, and summed to obtain the average daily integral of PPFD for each leaf to characterize its insolation regime. Also measured were leaf N per area (N(area)), leaf mass per area (LMA), the cosine of leaf inclination and the parameters of the photosynthetic light response curve [photosynthetic capacity (A(max)), dark respiration (R(d)), apparent quantum yield (phi) and curvature (theta)]. The instantaneous PPFD measurements and light response curves were used to estimate leaf daily photosynthesis (A(daily)) for each leaf.

Key results: Leaf N(area) and A(max) changed as a hyperbolic asymptotic function of the PPFD regime, not the linear relationship predicted by ONA. Despite this suboptimal nitrogen partitioning among leaves, A(daily) did increase linearly with PPFD regime through co-ordinated adjustments in both leaf angle and physiology along canopy gradients in insolation, exhibiting a strong convergence among the three species.

Conclusions: The results suggest that canopy tree leaves in this tropical forest optimize photosynthetic use of PPFD rather than N per se. Tropical tree canopies then can be considered simple 'big-leaves' in which all constituent 'small leaves' use PPFD with the same photosynthetic efficiency.

Fig. 1.

Relationships between leaf nitrogen content (g m⁻²) of individual leaves vs. PPFD regime (mol m⁻² d⁻¹; left-hand panels) and leaf photosynthetic capacity (A_max, μmol m⁻² s⁻¹) of individual leaves vs. PPFD regime (right-hand panels) in five tropical canopy trees. The PPFD regime was calculated as average daily PPFD incident on the adaxial surface of individual leaves at their natural orientation. The continuous lines correspond to two-parameter hyperbolas with both parameters significantly different from zero. ‘FI’ refers to Ficus insipida (individuals 1 and 2), ‘CE’ to Castilla elastica (individuals 1 and 2) and ‘LS’ to Luehea seemannii.

Fig. 2.

Relationships between leaf mass per area (LMA, g m⁻²) of individual leaves vs. PPFD regime (mol m⁻² d⁻¹; left-hand panels) and leaf dark respiration (R_d, μmol m⁻² s⁻¹) vs. PPFD regime (right-hand panels) in five tropical canopy trees. The continuous lines show the best fit to a two-parameter hyperbola with both parameters significantly different from zero, while the dashed line is for relationships with at least one parameter not different from zero. See Fig. 1 for species’ names.

Fig. 3.

Relationships between cosine of leaf angle and PPFD regime (mol m⁻² d⁻¹) of individual leaves vs. PPFD regime in five tropical canopy trees. Cosine of leaf angle was calculated by taking the product of the cosine of the angle of rotation and the cosine of the angle of inclination of the leaf blade (see Materials and Methods). Leaves with a cosine of 1·0 were horizontal while leaves with a cosine of 0·0 were fully vertical. Continuous lines correspond to statistically significant least square linear regressions. The dashed line is for a non-significant relationship. See Fig. 1 for species’ names.

Fig. 4.

Linear regressions between the PPFD regime (mol m⁻² d⁻¹) of individual leaves and average daily net leaf photosynthesis (A_daily, mol m⁻² d⁻¹) for five tropical canopy trees. Regression slopes and intercepts did not differ among the five trees (see Results). Each point corresponds to an individual leaf for which average daily net photosynthesis was calculated for the period of PPFD measurements (between 9 and 17 d). See Fig. 1 for species’ names.

Fig. 5.

Relationship between leaf nitrogen content (g m⁻²) and leaf daytime carbon gain (A_daily, mol m⁻² d⁻¹; left panel) and between leaf photosynthetic capacity (A_max, μmol m⁻² s⁻¹) and A_daily (right panel). The continuous lines correspond to statistically significant least square exponential regressions. See Fig. 1 for species’ names.