Original Articles

The Effects of Nitrogen Limitation on Ter r estr ial Ecosystem Carbon Cycle: a Review

  • 1. Institute of Geographical Sciences and Natural Resources Research, CAS, Beijing 100101, China|
    2. Graduate School of the Chinese Academy of Sciences (GSCAS), Beijing 100038

Received date: 2006-03-01

  Revised date: 2006-06-01

  Online published: 2006-07-25


Terrestrial carbon cycle and nitrogen cycle are closely coupled. Some factors, such as temperature, water and CO2 concentration, were more considered in the previous carbon researches than the nitrogen because of the complexity of nitrogen cycle, but this situation has changed in recent years. Nitrogen has great effects on the plant photosynthesis, organic matter decomposition, carbon allocation and the responses of ecosystem when the atmospheric CO2 concentration increases. There are generally three types of carbon models to consider nitrogen limitation on carbon assimilation: (1) static models: these type models usually use a constant soil fertility index or leaf nitrogen concentration and are fit for a site or district where the nitrogen variability can be neglected; (2) soil nitrogen limitation models: these models can maintain stable nitrogen budgets and dynamic soil nitrogen can turn the potential NPP to actual NPP; (3) leaf nitrogen limitation models: such models are similar to soil nitrogen limitation but feature a further dynamic leaf- level nitrogen regulation of NPP. The common approach uses relative leaf nitrogen concentration to scale down proportionally either the maximum Rubisco or the NPP. Although the three type models all consider the nitrogen effects on carbon cycle, they may produce great uncertainty in carbon research because of the partly understanding of the interaction between carbon and nitrogen. Future studies should focus on both the experiment and observation about the nitrogen feedbacks on carbon cycle and the development of integrated dynamic ecosystem models that can describe the interaction of carbon and nitrogen cycle, contributing to decreasing the uncertainty in the carbon research.

Cite this article

REN Shujie,CAO Mingkui,TAO Bo,LI Kerang . The Effects of Nitrogen Limitation on Ter r estr ial Ecosystem Carbon Cycle: a Review[J]. PROGRESS IN GEOGRAPHY, 2006 , 25(4) : 58 -67 . DOI: 10.11820/dlkxjz.2006.04.007


[1] 于贵瑞主编. 全球变化与陆地生态系统碳循环和碳蓄积. 北京: 气象出版社.2003: 1~460.

[2] Redfield A C. The biological control of chemical factors in the environment. American Scientist, 1958, 46: 205~221.

[3] Broecker W S, Takahashi T, Simpson L G, et al. Fate of fossil fuel carbon dioxide and the global carbon budget. Science, 1979, 206: 409~418.

[4] Vitousek P M. Nutrient cycling and nutrient use efficiency. American Naturalist, 1982, 119: 53~72.

[5] Vitousek P M, Howarth R W. Nitrogen limitation on land and in the sea: How can it occur? Biogeochemistry, 1991, 13: 87~115.

[6] Liu J X, Price D T, Chen J M. Nitrogen controls on ecosystem carbon sequestration: a model implementation and application to Saskatchewan, Canada. Ecological modeling, 2005, 186: 178~195.

[7] Cleveland C C, Townsend A R, Schimel D S, et al. Global patterns of terrestrial biological nitrogen (N2) fixation in natural ecosystems. Global Biogeochemical Cycles, 1999, 13: 623~645.

[8] Galloway J N, Dentener F J, Capone D G, et al. Nitrogen cycles: past, present, and future. Biochemistry, 2004, 70: 153~ 226.

[9] Lelieveld J, Dentener F J. What controls troposphere ozone? Journal of Geophysical Research, 2000, 105: 3531~3551.

[10] Prather M, Ehalt D, Dentener F, et al. Atmospheric chemistry and greenhousegases. 2001. In: Houghton J T, Ding Y, Griggs D J, et al. (eds), Climate change 2001: the scientific basis. Third Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, NY.

[11] Kramer DA. Minerals Yearbook. Nitrogen. US Geological Survey Minerals Information. 1999. Http://minerals.usgs.gov/minerals/ pubs/commodity/nitrogen.

[12] Van Aardenne J A, Dentener F J, Olivier J G J, et al. A 1°~1°resolution dataset of historical anthropogenic trace gas emissions for the period 1890~1990. Global Biogeochemical Cycles, 2001, 15: 909~928.

[13] 郭盛磊, 阎秀峰, 白冰等. 落叶松幼苗光合特性对氮和磷缺乏的响应. 应用生态学报, 2005, 16(4): 589~594.

[14] 李卫民, 周凌云. 水肥(氮) 对小麦生理生态的影响(Ⅰ)水肥(氮) 条件对小麦光合蒸腾与水分利用的影响. 土壤通报, 2004, 35(2): 136~142.

[15] 徐克章. 水稻开花后叶片含氮量与光合作用的动态变化及其关系. 作物学报, 1995, 21(2): 171~175.

[16] Anten N P R, Schieving F, Werger M J A. Patterns of light and nitrogen distribution in relation to whole canopy carbon gain in C3 and C4 mono~ and dicotyledonous species. Oecologia, 1995, 101: 504~513.

[17] Anten N P R, Werger M J A, Medina E. Nitrogen distribution and leaf area indices in relation to photosynthetic nitrogen use efficiency in savanna grasses. Plant Ecology, 1998, 138: 63~75.

[18] Thompson W A, Wheeler A M. Photosynthesis by nature needles of field~grown Pinus radiata. Forest Ecology and Management, 1992, 52: 225~242.

[19] Dickinson R E, Berry J A, Bonan G B, et al. Nitrogen Controls on climate model evapotranspiration. Journal of Climate, 2002, 15: 278~295.

[20] Moorhead D L, Reynolds J F. A general model of litter decomposition in the northern Chihuahuan desert. Ecological Modelling, 1991, 56: 197~219.

[21] 黄昌勇主编. 土壤学. 北京: 中国农业出版社, 2000: 1~311.

[22] Nikli#ska M, Marya$ski M, Laskowski R. Effect of temperature on humus respiration rate and nitrogen mineralization: implication for global climate change. Biogeochemistry, 1999, 44: 239~257.

[23] Meentemeyer V. An approach to the biometeorology of decomposer organisms. International Journal of Biometeorology, 1978, 22: 94~102.

[24] Melillo J M, Gosz J R. Interactions of biogeochemical cycles in forest ecosystems. In: The major biogeochemicalcycles and their interactions. Bolin B and Cook R B (Eds.). John Wiley and Sons, New York, 1983, 177~222.

[25] Norby R J. Nitrogen deposition: a component of global change analyses. New Phytologist, 1998, 139(1): 189~200.

[26] K%rner C. Biosphere responses to CO2 enrichment. Ecological Applications. 2000, 10: 1590~1619.

[27] Rastetter E B, Ryan M G, Shaver G R, et al. A general biogeochemical model describing the responses of the C and N cycles in terrestrial ecosystems to changes in CO2, climate, and N deposition. Tree Physiology, 1991, 9: 101~126.

[28] Tilman D. Plant strategies and the dynamics and structure of plant communities. Princeton University Press, Princeton, NJ. 1988.

[29] Friedlingstein P, Joel G, Field C B, et al. Toward an Allocation Scheme for Global Terrestrial Carbon Models. Global Change Biology, 1999, 5: 755~770.

[30] Shinozaki K, Yoda K, Hozumi K et al. A quantitative analysis of plant form- the pipe model theory: I. Basic Analyses. Japanese Journal of Ecology, 1964, 14: 97~103.

[31] Woodward F I, Smith T M, Emanuel W R. A global land primary productivity and phytogeography model. Global Biogeochemical Cycles, 1995, 9: 471~490.

[32] Wilson J B. A review of evidence in the control of root:shoot ratios in relation to models. Annals of Botany, 1988, 61: 433~ 449.

[33] Cannell M G R, Dewar R C. Carbon allocation in trees: a review of concepts for modeling. Advances in Ecological Research, 1994, 25: 59~104.

[34] Beets P N, Whitehead D. Carbon partitioning in Pinus radiata stands in relation to foliage nitrogen status Tree Physiology, 1996, 16: 139~144.

[35] Shangguan Z P, Shao M A, Ren S J, et al. Effect of Nitrogen on Root and Shoot Relations and Gas Exchange in Winter wheat. Botanical Bulletin of Academia Sinica, 2004, 45: 49~54.

[36] Runyon J, Waring R H, Goward S N, et al. Environmental limits on net primary production and light- use efficiency across the Oregon transect. Ecological Applications, 1994, 4: 226~237.

[37] Cao M K, Woodward F I. Dynamic responses of terrestrial ecosystem carbon cycling to global climate change. Nature, 1998, 393: 249~252.

[38] Webber A N, Nie G Y, Long S P. Acclimation of photosynthetic proteins to rising atmospheric CO2. Photosynthesis Research, 1994, 39(3): 413~425.

[39] Rogers H H, Prior S A, Runion G B, et al. Root to shoot ratio of crops as influenced by CO2. Plant and Soil, 1996, 187(2): 229~248.

[40] Houghton R A, Davidson E A, Woodwell G M. Missing sinks, feedbacks, and understanding the role of terrestrial ecosystems in the global carbon balance. Global Biogeochemical Cycles, 1998, 12: 25~34.

[41] Chen W, Chen J M, Cihlar J. An integrated terrestrial ecosystem carbon- budget model based on changes in disturbance, climate, and atmospheric chemistry. Ecological Modelling, 2000, 135: 55~79.

[42] Schlesinger W H, Lichter J. Limited carbon storage in soil and litter of experimental forest plots under elevated atmospheric CO2. Nature, 2001, 411: 466~469.

[43] Oren R R, Ellsworth D S, Johnsen K H, et al. Soil fertility limits carbon sequestration by forest ecosystems in a CO2- enriched atmosphere. Nature, 2001: 469~472.

[44] McGuire A D, Melillo J M, Joyce L A. The role of nitrogen in the response of forest net primary production to elevated atmospheric carbon dioxide. Annual Review of Ecology and Systematics, 1995, 26: 473~503.

[45] Poorter H, Pérez~Soba M. The growth response of plants to elevated CO2 under non~optimal environmental conditions. Oecologia, 2001, 129: 1~20.

[46] Hungate B A, Dukes J S, ShawMR, et al. Nitrogen and Climate Change. Science, 2003, 302: 1512~1513.

[47] Paavolainen L. Nitrogen transformations in boreal forest soils in response to extreme manipulation treatments. Academic Dissertation in Environmental Microbiology. Faculty of Agriculture and Forestry University of Helsinki, Helsinki, 1999.

[48] Hobbie S E, Nadelhoffer K J, H#ogberg P. A synthesis: the role of nutrients as constraints on carbon balances in boreal and arctic regions. Plant and Soil, 2002, 242: 163~170.

[49] Vitousek P M, Aber J D, Howarth R W, et al. Human alteration of the global nitrogen cycle: Sources and consequences. Ecological applications, 1997, 7:737~750.

[50] Houghton R A, Woodwell G M. Global climatic change. Scientific American, 1989, 260(4): 36~47.

[51] Watson R T, Rodhe H, Oeschger H, et al. In climate change: The IPCC Scientific Assessment. Eds. Houghton J T, Jenkins G J, Ephraums J J. Cambridge University Press, Cambridge. 1990.

[52] Houghton R A, Jenkins G J, Ephraums J J (eds). Climate Change: The IPCC Scientific Assessment. Cambridge: Cambridge University Press, 1990, 1~150.

[53] McGuire A D, Melillo J M, Joyce L A, et al. Interactions between carbon and nitrogen dynamics in estimating net primary productivity for potential vegetation in North America. Global Biogeochemical Cycles, 1992, 6: 101~124.

[54] Raich J W, Rastetter E B, Melillo J M, et al. Potential net primary productivity in South America: application of a global model. Ecological Applications, 1991, 1: 399~429.

[55] VEMAP Members. Vegetation/ecosystem modeling and analysis project: Comparing biogeography and biogeochemistry models in a continental - scale study of terrestrial ecosystem responses to climate change and CO2 doubling. Global Biogeochemical Cycles, 1995, 4: 407~437.

[56] Bousquet P, Peylin P, Ciais P, et al. Regional changes in carbon dioxide fluxes of land and oceans since 1980. Science, 2000, 290: 1342~1346.

[57] Melillo J M, McGuire A D, Kicklighter D W, et al. Productivity response of climax temperate forests to elevated temperature and carbon dioxide: a North American comparison between two global models. Climate change, 1993, 24: 287~310.

[58] Running S W, Hunt E R. Generalization of a forest ecosystem process model for other biomes, BIOME- BGC, and an application for global –scale models, Scaling processes between leaf and landscape levels. In: scaling physiological Processes: Leaf to Globe. Academic Press, San Diego. 1993. PP. 141~158.

[59] Schimel D, Alves D, Enting I, et al. CO2 and the carbon cycle. In: Houghton J T, Meira Filho L G, Callander B A, et al. (Eds.). Climate change 1995; the science of climate change: Contribution of WGI to the Second Assessment Report of the IPCC. Cambridge University Press, Cambridge. 1996a, PP. 65~86.

[60] Cao M K, Woodward FI. Net primary and ecosystem production and carbon stocks of terrestrial ecosystems and their response to climatic change, Global Change Biology, 1998, 4: 185~198.

[61] Melillo J M, Prentice I C, Farquhar G D, et al. Terrestrial biotic response to environmental change and feedbacks to climate, In: Houghton JT, Filho L G M, Callander B B, Harris N, et al. (Eds.). Climate Change 1995. The science of Climate change. University press, Cambridge. 1996, PP. 449~481.

[62] 李克让主编. 土地利用变化和温室气体排放与陆地生态系统碳循环. 北京: 气象出版, 2002, 1~310.

[63] 汪业勖, 赵士洞. 陆地碳循环研究中的模拟方法. 应用生态学报, 1998, 9(6): 658~664.

[64] Asner G P, Townsend A R, Riley W, et al. Physical and biogeochemical controls of terrestrial ecosystems responses to nitrogen deposition. Biogeochemistry, 2001, 54: 1~39.

[65] Landsberg J J, Waring R H. A generalized model of forest productivity using simplified concepts of radiation- use efficiency, carbon balance and partitioning. Forest Ecology and Management, 1997, 95: 209~228.

[66] Sellers J P, Randell D A, Collatz G J, et al. A revised land surface parameterization (SiB 2) for atmospheric GCMs. Part I. Model formulation. Journal of Climate, 1996, 9, 676~705.

[67] Warnant P, Franccois L, Strivay D, et al.. CARAIB: a global model of terrestrial biological productivity. Global Biogeochemical Cycles, 1994, 8: 255~270.

[68] Haxeltine A, Prentice I C. BIOME3: an equilibrium terrestrial biosphere model based on ecophysiological constraints, resource availability and competition among plant functional types. Global Biogeochemical Cycles, 1996, 10: 693~709.

[69] Parton W J, Schimel D S, Cole C V, et al. Analysis of factors controlling soil organic matter levels in Great Plains grasslands. Soil Science Society of America Journal, 1987, 51: 1173~1179.

[70] Schimel D S, Braswell B H, McKeown R, et al. Climate and nitrogen controls on the geography and timescales of terrestrial biogeochemical cycling. Global Biogeochemical Cycles, 1996, 10 (4): 677~692.

[71] Bossel H. TREEDYN3 Forest Simulation Model - mathematical model, program documentation, and simulation results. Forschungszentrum Wald#kosysteme der Univ. Goettingen, Goettingen, B35, 1994.

[72] Farquhar G D, von Caemmerer S, Berry J A. A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta, 1980, 149: 78~90.

[73] Friend A D, Stevens A K, Knox R G, et al. A process- based, terrestrial biosphere model of ecosystem dynamics (Hybrid 3.0). Ecological Modelling, 1997, 95: 249~287.

[74] Running S W, Coughlan J C. A general model of forest ecosystem processes for regional applications. I. Hydrologic balance canopy gas exchange and primary production processes. Ecological Modelling, 1988, 42: 125~154.

[75] Running S W, Gower S T. FOREST- BGC, a general model of forest ecosystem processes for regional applications. II. Dynamic carbon allocation and nitrogen budgets. Tree Physiology. 1991, 9: 147~160.

[76] Kirschbaum M U F, Cen W. A forest growth model with linked carbon, energy, nutrient and water cycles. Ecological Modelling, 1999, 118: 17~59.

[77] Verseghy D L, McFarlane N A, Lazare M. CLASS- a Canadian land surface scheme for GCMs, II. Vegetation model and coupled runs. International Journal of Climatology, 1993, 13: 347~370.

[78] Wang S, Grant R F, Verseghy D L, et al. Modelling plant carbon and nitrogen dynamics of a boreal aspen forest in CLASS- the Canadian land surface scheme. Ecological Modelling, 2001, 142: 135~154.

[79] Canadell J G, Mooney H A, Baldocchi D D, et al. Carbon metabolism of the terrestrial biosphere: A multi~technique approach for improved understanding. Ecosystems, 2000, 3: 115~130.

[80] Norby R J, Lou Y Q. Evaluating ecosystem responses to rising atmospheric CO2 and global warming in a multi - factor world. 2004, 162: 281~293.

[81] Sterner R W, Elser J J. Ecological Stoichiometry. In the United Kingdom: Princeton University Press. 2002.

[82] He J S, Flynn D F B, Wolfe- Bellin K, et al. CO2 and nitrogen, but not population density, alter the size and C/N ratio of Phytolacca Americana seeds. Functional Ecology, 2005, 19: 437~444.