Toward a Mechanistic Modeling of Nitrogen Limitation on Vegetation Dynamics

Nitrogen is a dominant regulator of vegetation dynamics, net primary production, and terrestrial carbon cycles; however, most ecosystem models use a rather simplistic relationship between leaf nitrogen content and photosynthetic capacity. Such an approach does not consider how patterns of nitrogen allocation may change with differences in light intensity, growing-season temperature and CO2 concentration. To account for this known variability in nitrogen-photosynthesis relationships, we develop a mechanistic nitrogen allocation model based on a trade-off of nitrogen allocated between growth and storage, and an optimization of nitrogen allocated among light capture, electron transport, carboxylation, and respiration. The developed model is able to predict the acclimation of photosynthetic capacity to changes in CO2 concentration, temperature, and radiation when evaluated against published data of Vc,max (maximum carboxylation rate) and Jmax (maximum electron transport rate). A sensitivity analysis of the model for herbaceous plants, deciduous and evergreen trees implies that elevated CO2 concentrations lead to lower allocation of nitrogen to carboxylation but higher allocation to storage. Higher growing-season temperatures cause lower allocation of nitrogen to carboxylation, due to higher nitrogen requirements for light capture pigments and for storage. Lower levels of radiation have a much stronger effect on allocation of nitrogen to carboxylation for herbaceous plants than for trees, resulting from higher nitrogen requirements for light capture for herbaceous plants. As far as we know, this is the first model of complete nitrogen allocation that simultaneously considers nitrogen allocation to light capture, electron transport, carboxylation, respiration and storage, and the responses of each to altered environmental conditions. We expect this model could potentially improve our confidence in simulations of carbon-nitrogen interactions and the vegetation feedbacks to climate in Earth system models.

[1]  R. Dewar,et al.  Leaf-trait variation explained by the hypothesis that plants maximize their canopy carbon export over the lifespan of leaves. , 2011, Tree physiology.

[2]  Markus Reichstein,et al.  Improving canopy processes in the Community Land Model version 4 (CLM4) using global flux fields empirically inferred from FLUXNET data , 2011 .

[3]  Charles W. Cook,et al.  Re-assessment of plant carbon dynamics at the Duke free-air CO(2) enrichment site: interactions of atmospheric [CO(2)] with nitrogen and water availability over stand development. , 2010, The New phytologist.

[4]  Qianlai Zhuang,et al.  A global sensitivity analysis and Bayesian inference framework for improving the parameter estimation and prediction of a process-based Terrestrial Ecosystem Model , 2009 .

[5]  Ian J. Wright,et al.  Leaf phosphorus influences the photosynthesis–nitrogen relation: a cross-biome analysis of 314 species , 2009, Oecologia.

[6]  Harry T. Valentine,et al.  Optimal Function Explains Forest Responses to Global Change , 2009 .

[7]  Y. Malhi,et al.  Carbon cost of plant nitrogen acquisition: A mechanistic, globally applicable model of plant nitrogen uptake, retranslocation, and fixation , 2010 .

[8]  D. Ellsworth,et al.  Elevated CO(2) concentration affects leaf photosynthesis-nitrogen relationships in Pinus taeda over nine years in FACE. , 2008, Tree physiology.

[9]  K. Treseder,et al.  Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. , 2008, Ecology.

[10]  K. Seiwa.  Trade-offs between seedling growth and survival in deciduous broadleaved trees in a temperate forest. , 2007, Annals of botany.

[11]  R. Ceulemans,et al.  Forest response to elevated CO2 is conserved across a broad range of productivity. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[12]  M. Wassen,et al.  A simple model for nitrogen-limited plant growth and nitrogen allocation. , 2005, Annals of botany.

[13]  K. Hikosaka.  Nitrogen partitioning in the photosynthetic apparatus of Plantago asiatica leaves grown under different temperature and light conditions: similarities and differences between temperature and light acclimation. , 2005, Plant & cell physiology.

[14]  D. Kleijn,et al.  The importance of nitrogen and carbohydrate storage for plant growth of the alpine herb Veratrum album. , 2005, The New phytologist.

[15]  S. Long,et al.  What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. , 2004, The New phytologist.

[16]  A. Rogers,et al.  Rising atmospheric carbon dioxide: plants FACE the future. , 2004, Annual review of plant biology.

[17]  P. Reich,et al.  Different photosynthesis-nitrogen relations in deciduous hardwood and evergreen coniferous tree species , 1995, Oecologia.

[18]  J. Berry,et al.  A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species , 1980, Planta.

[19]  I. Stulen,et al.  Enzymes of nitrogen assimilation in maize roots , 1980, Planta.

[20]  J. R. Evans.  Photosynthesis and nitrogen relationships in leaves of C3 plants , 2004, Oecologia.

[21]  S. Long,et al.  Review Tansley Review , 2022 .

[22]  M. Adams,et al.  Photosynthesis-Rubisco relationships in foliage of Pinus sylvestris in response to nitrogen supply and the proposed role of Rubisco and amino acids as nitrogen stores , 2003, Trees.

[23]  G. Grassi,et al.  Photosynthesis-nitrogen relationships: interpretation of different patterns between Pseudotsuga menziesii and Populus x euroamericana in a mini-stand experiment. , 2003, Tree physiology.

[24]  Peter E. Thornton,et al.  Modeling and measuring the effects of disturbance history and climate on carbon and water budgets in evergreen needleleaf forests , 2002 .

[25]  P. Ineichen,et al.  A new operational model for satellite-derived irradiances: description and validation , 2002 .

[26]  D. Ellsworth,et al.  Photosynthetic acclimation of Pinus taeda (loblolly pine) to long‐term growth in elevated pCO2 (FACE) , 2002 .

[27]  F. Stuart Chapin,et al.  Species composition interacts with fertilizer to control long-term change in tundra productivity , 2001 .

[28]  John R. Evans,et al.  Photosynthetic acclimation of plants to growth irradiance: the relative importance of specific leaf area and nitrogen partitioning in maximizing carbon gain , 2001 .

[29]  Tsuyoshi Kobayashi,et al.  Variations in size structure, growth and reproduction in Japanese plantain (Plantago asiatica L.) between exposed and shaded populations , 2001 .

[30]  Peter E. Thornton,et al.  Parameterization and Sensitivity Analysis of the BIOME–BGC Terrestrial Ecosystem Model: Net Primary Production Controls , 2000 .

[31]  P. De Angelis,et al.  Effects of elevated (CO2) on photosynthesis in European forest species: a meta-analysis of model parameters , 1999 .

[32]  Olevi Kull,et al.  An analysis of light effects on foliar morphology, physiology, and light interception in temperate deciduous woody species of contrasting shade tolerance. , 1998, Tree physiology.

[33]  O. Kull,et al.  Stoichiometry of foliar carbon constituents varies along light gradients in temperate woody canopies: implications for foliage morphological plasticity. , 1998, Tree physiology.

[34]  P. Haldimann.  Low growth temperature‐induced changes to pigment composition and photosynthesis in Zea mays genotypes differing in chilling sensitivity , 1998 .

[35]  Ü. Niinemets.  Role of foliar nitrogen in light harvesting and shade tolerance of four temperate deciduous woody species , 1997 .

[36]  S. Ollinger,et al.  Modeling nitrogen saturation in forest ecosystems in response to land use and atmospheric deposition , 1997 .

[37]  John Tenhunen,et al.  A model separating leaf structural and physiological effects on carbon gain along light gradients for the shade‐tolerant species Acer saccharum , 1997 .

[38]  A. Nordin,et al.  Nitrogen storage forms in nine boreal understorey plant species , 1997, Oecologia.

[39]  Peter E. Thornton,et al.  Generating surfaces of daily meteorological variables over large regions of complex terrain , 1997 .

[40]  K. Hikosaka,et al.  Nitrogen partitioning among photosynthetic components and its consequence in sun and shade plants , 1996 .

[41]  G. Edwards,et al.  Carbon Metabolism and Photorespiration: Temperature Dependence in Relation to Other Environmental Factors , 1996 .

[42]  Ichiro Terashima,et al.  A model of the acclimation of photosynthesis in the leaves of C3 plants to sun and shade with respect to nitrogen use , 1995 .

[43]  A. Makino,et al.  Effects of Growth Temperature on the Responses of Ribulose-1,5-Biphosphate Carboxylase, Electron Transport Components, and Sucrose Synthesis Enzymes to Leaf Nitrogen in Rice, and Their Relationships to Photosynthesis , 1994, Plant physiology.

[44]  D. Herms,et al.  The Dilemma of Plants: To Grow or Defend , 1992, The Quarterly Review of Biology.

[45]  A. Holaday,et al.  Changes in Activities of Enzymes of Carbon Metabolism in Leaves during Exposure of Plants to Low Temperature. , 1992, Plant physiology.

[46]  H. Poorter,et al.  Chemical composition of 24 wild species differing in relative growth rate , 1992 .

[47]  A. Friend.  Use of a model of photosynthesis and leaf microenvironment to predict optimal stomatal conductance and leaf nitrogen partitioning , 1991 .

[48]  B. Osmond,et al.  Effects of Nitrogen Nutrition on Nitrogen Partitioning between Chloroplasts and Mitochondria in Pea and Wheat. , 1991, Plant physiology.

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

[50]  H. Lambers,et al.  Carbon and nitrogen economy of 24 wild species differing in relative growth rate. , 1990, Plant physiology.

[51]  F. Stuart Chapin,et al.  The Ecology and Economics of Storage in Plants , 1990 .

[52]  P. Millard.  The accumulation and storage of nitrogen by herbaceous plants , 1988 .

[53]  T. Sharkey,et al.  Environmental effects on photosynthesis, nitrogen-use efficiency, and metabolite pools in leaves of sun and shade plants. , 1987, Plant physiology.

[54]  H. Marschner.  Mineral Nutrition of Higher Plants , 1988 .

[55]  F. Stuart Chapin,et al.  Individualistic Growth Response of Tundra Plant Species to Environmental Manipulations in the Field , 1985 .

[56]  H. Mooney,et al.  Resource Limitation in Plants-An Economic Analogy , 1985 .

[57]  James R. Ehleringer,et al.  Quantum Yields for CO2 Uptake in C3 and C4 Plants: Dependence on Temperature, CO2, and O2 Concentration , 1977 .

[58]  W. K. Hastings,et al.  Monte Carlo Sampling Methods Using Markov Chains and Their Applications , 1970 .

[59]  D. Bendall.  Cytochromes and some respiratory enzymes in mitochondria from the spadix of Arum maculatum. , 1958, The Biochemical journal.

[60]  N. Metropolis,et al.  Equation of State Calculations by Fast Computing Machines , 1953, Resonance.