Leaf structure (specific leaf area) modulates photosynthesis–nitrogen relations: evidence from within and across species and functional groups

1. Net photosynthetic capacity (Amax, defined as light-saturated net photosynthesis under near optimal ambient environmental conditions) of mature leaves often depends on the level of leaf nitrogen (N), but an assortment of relationships between these variables has been observed in studies of diverse plant species. Variation in leaf structure has been identified as an important factor associated with differences between the area- and mass-based expressions of the Amax–N relationship. In this paper we test the hypothesis that leaf structure, quantified using a measure of leaf area displayed per unit dry mass invested [specific leaf area (SLA)], is more than just a conversion factor, but itself can influence Amax–N relationships. We test this using several kinds of comparisons, based on field data for 107 species from sites representing six biomes and on literature data for 162 species from an equally diverse set of biomes. 2. Species and genera with thicker and/or denser leaves (lower SLA) consistently have flatter slopes of the Amax–N (mass-based) relationship than those with higher SLA. These and all other contrasts usually applied as well using area-based expressions, although such relationships were less consistent and weaker overall. A steeper slope indicates greater incremental change in Amax per unit variation in N. 3. Functional groups (e.g. needle-leafed evergreen trees, broad-leafed trees or shrubs, forbs) show the same patterns: groups with lower SLA have lower Amax–N slopes. Functional groups differ in mean leaf traits as well as in Amax–N relationships. Forbs have the highest SLA and mass-based N and Amax, followed by deciduous species (whether needle-leafed or broad-leafed, shrub or tree), with lowest values in evergreen species (again regardless of leaf type or functional group). 4. Interspecific variation in mass-based Amax is highly significantly related to the combination of leaf N and SLA (r2 = 0·86). At any value of leaf N, Amax increases with increasing SLA and at any value of SLA, Amax increases with increasing leaf N. Because this relationship, between Amax and the combination of N and SLA, is similar in two independent data sets, and as well, across broad taxonomic and geographic gradients, we hypothesize that it is universal in nature. Therefore, for broad interspecific contrasts among dicotyledons in any biome, we can reasonably well predict Amax based on the combination of SLA and leaf N. These findings have important implications for convergent evolution of leaf adaptation and great potential utility in models of global vegetation functioning.

[1]  Mark G. Tjoelker,et al.  Growth and physiology of Picea abies populations from elevational transects: common garden evidence for altitudinal ecotypes and cold adaptation , 1998 .

[2]  M. Navas.  Individual species performance and response of multi‐specific communities to elevated CO2: a review , 1998 .

[3]  P. Reich,et al.  Relationships of leaf dark respiration to leaf nitrogen, specific leaf area and leaf life-span: a test across biomes and functional groups , 1998, Oecologia.

[4]  P. Reich,et al.  Generality of leaf trait relationships: a test across six biomes: Ecology , 1999 .

[5]  P. Reich,et al.  Leaf age and season influence the relationships between leaf nitrogen, leaf mass per area and photosynthesis in maple and oak trees , 1991 .

[6]  M. Abrams,et al.  Relating Wet and Dry Year Ecophysiology to Leaf Structure in Contrasting Temperate Tree Species , 1994 .

[7]  R. Sage,et al.  The Nitrogen Use Efficiency of C(3) and C(4) Plants: II. Leaf Nitrogen Effects on the Gas Exchange Characteristics of Chenopodium album (L.) and Amaranthus retroflexus (L.). , 1987, Plant physiology.

[8]  A. McGuire,et al.  Global climate change and terrestrial net primary production , 1993, Nature.

[9]  Thomas J. Givnish,et al.  On the economy of plant form and function. , 1988 .

[10]  P. Reich,et al.  Leaf Life‐Span in Relation to Leaf, Plant, and Stand Characteristics among Diverse Ecosystems , 1992 .

[11]  P. Reich,et al.  Photosynthesis and leaf nitrogen in five Amazonian tree species during early secondary succession , 1996 .

[12]  J. Hesketh,et al.  Photosynthesis among Species in Relation to Characteristics of Leaf Anatomy and CO2 Diffusion Resistance1 , 1965 .

[13]  P. Reich.  Reconciling apparent discrepancies among studies relating life span, structure and function of leaves in contrasting plant life forms and climates: the blind men and the elephant retold' , 1993 .

[14]  G. Collatz,et al.  Physiological and environmental regulation of stomatal conductance, photosynthesis and transpiration: a model that includes a laminar boundary layer , 1991 .

[15]  P. Reich,et al.  Needle CO2 exchange, structure and defense traits in relation to needle age in Pinus heldreichii Christ – a relict of Tertiary flora , 1997, Trees.

[16]  Ichiro Terashima,et al.  Comparative ecophysiology of leaf and canopy photosynthesis , 1995 .

[17]  F. Woodward,et al.  Predictions and Measurements of the Maximum Photosynthetic Rate, Amax, at the Global Scale , 1995 .

[18]  G. Farquhar,et al.  Low conductances for CO2 diffusion from stomata to the sites of carboxylation in leaves of woody species , 1992 .

[19]  Stan D. Wullschleger,et al.  Biochemical Limitations to Carbon Assimilation in C3 Plants—A Retrospective Analysis of the A/Ci Curves from 109 Species , 1993 .

[20]  E. Garnier,et al.  Leaf anatomy, specific mass and water content in congeneric annual and perennial grass species , 1994 .

[21]  P. Reich,et al.  Leaf mass per area, nitrogen content and photosynthetic carbon gain in Acer saccharum seedlings in contrasting forest light environments , 1992 .

[22]  D. F. Parkhurst,et al.  Diffusion of CO2 and other gases inside leaves. , 1994, The New phytologist.

[23]  P. Reich,et al.  From tropics to tundra: global convergence in plant functioning. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[24]  D. Epron,et al.  Limitation of net CO2 assimilation rate by internal resistances to CO2 transfer in the leaves of two tree species (Fagus sylvatica L. and Castanea sativa Mill.) , 1995 .