Forest productivity under elevated CO₂ and O₃: positive feedbacks to soil N cycling sustain decade-long net primary productivity enhancement by CO₂.

The accumulation of anthropogenic CO₂ in the Earth's atmosphere, and hence the rate of climate warming, is sensitive to stimulation of plant growth by higher concentrations of atmospheric CO₂. Here, we synthesise data from a field experiment in which three developing northern forest communities have been exposed to factorial combinations of elevated CO₂ and O₃. Enhanced net primary productivity (NPP) (c. 26% increase) under elevated CO₂ was sustained by greater root exploration of soil for growth-limiting N, as well as more rapid rates of litter decomposition and microbial N release during decay. Despite initial declines in forest productivity under elevated O₃, compensatory growth of O₃ -tolerant individuals resulted in equivalent NPP under ambient and elevated O₃. After a decade, NPP has remained enhanced under elevated CO₂ and has recovered under elevated O₃ by mechanisms that remain un-calibrated or not considered in coupled climate-biogeochemical models simulating interactions between the global C cycle and climate warming.

[1]  Yiqi Luo,et al.  Carbon and nitrogen dynamics during forest stand development: a global synthesis. , 2011, The New phytologist.

[2]  R. B. Jackson,et al.  Increases in the flux of carbon belowground stimulate nitrogen uptake and sustain the long-term enhancement of forest productivity under elevated CO₂. , 2011, Ecology letters.

[3]  E. Bernhardt,et al.  Enhanced root exudation induces microbial feedbacks to N cycling in a pine forest under long-term CO2 fumigation. , 2011, Ecology letters.

[4]  D. Ort,et al.  Differential responses in two varieties of winter wheat to elevated ozone concentration under fully open‐air field conditions , 2011 .

[5]  S. Davis,et al.  Hydraulic limitation not declining nitrogen availability causes the age-related photosynthetic decline in loblolly pine (Pinus taeda L.). , 2010, Plant, cell & environment.

[6]  M. Lieffering,et al.  Ten years of elevated atmospheric carbon dioxide alters soil nitrogen transformations in a sheep‐grazed pasture , 2010 .

[7]  G. Wieser,et al.  Advances in understanding ozone impact on forest trees: messages from novel phytotron and free-air fumigation studies. , 2010, Environmental pollution.

[8]  A. Talhelm,et al.  Species-specific responses to atmospheric carbon dioxide and tropospheric ozone mediate changes in soil carbon. , 2009, Ecology letters.

[9]  R. Lindroth,et al.  Rising concentrations of atmospheric CO2 have increased growth in natural stands of quaking aspen (Populus tremuloides) , 2009 .

[10]  R. McMurtrie,et al.  CO2 enhancement of forest productivity constrained by limited nitrogen availability , 2009, Proceedings of the National Academy of Sciences.

[11]  S. Krupa,et al.  The ozone component of global change: potential effects on agricultural and horticultural plant yield, product quality and interactions with invasive species. , 2009, Journal of integrative plant biology.

[12]  K. Pregitzer,et al.  Soil respiration, root biomass, and root turnover following long-term exposure of northern forests to elevated atmospheric CO2 and tropospheric O3. , 2008, The New phytologist.

[13]  Peter E. Thornton,et al.  Influence of carbon‐nitrogen cycle coupling on land model response to CO2 fertilization and climate variability , 2007 .

[14]  K. Pregitzer,et al.  Atmospheric CO2 and O3 alter the flow of 15N in developing forest ecosystems. , 2007, Ecology.

[15]  D. Ellsworth,et al.  Belowground competition and the response of developing forest communities to atmospheric CO2 and O3 , 2007 .

[16]  R. B. Jackson,et al.  Increases in nitrogen uptake rather than nitrogen-use efficiency support higher rates of temperate forest productivity under elevated CO2 , 2007, Proceedings of the National Academy of Sciences.

[17]  C. Huntingford,et al.  Indirect radiative forcing of climate change through ozone effects on the land-carbon sink , 2007, Nature.

[18]  M. Kubiske,et al.  Effects of elevated atmospheric CO2 and/or O3 on intra- and interspecific competitive ability of aspen. , 2007, Plant biology.

[19]  P. Reich,et al.  Carbon-Nitrogen Interactions in Terrestrial Ecosystems in Response to Rising Atmospheric Carbon Dioxide , 2006 .

[20]  Johan Six,et al.  Interactions between plant growth and soil nutrient cycling under elevated CO2: a meta‐analysis , 2006 .

[21]  R. Schnur,et al.  Climate-carbon cycle feedback analysis: Results from the C , 2006 .

[22]  P. Reich,et al.  Nitrogen limitation constrains sustainability of ecosystem response to CO2 , 2006, Nature.

[23]  E. P. McDonald,et al.  Tropospheric O3 compromises net primary production in young stands of trembling aspen, paper birch and sugar maple in response to elevated atmospheric CO2 , 2005 .

[24]  John M. Reilly,et al.  Future Effects of Ozone on Carbon Sequestration and Climate Change Policy Using a Global Biogeochemical Model , 2005 .

[25]  K. Pregitzer,et al.  Scaling ozone responses of forest trees to the ecosystem level in a changing climate , 2005 .

[26]  Kurt S. Pregitzer,et al.  Carbon cycling and storage in world forests: biome patterns related to forest age , 2004 .

[27]  W. Parton,et al.  Progressive Nitrogen Limitation of Ecosystem Responses to Rising Atmospheric Carbon Dioxide , 2004 .

[28]  R. E. Dickson,et al.  Tropospheric O3 moderates responses of temperate hardwood forests to elevated CO2: a synthesis of molecular to ecosystem results from the Aspen FACE project , 2003 .

[29]  Denise L. Mauzerall,et al.  PROTECTING AGRICULTURAL CROPS FROM THE EFFECTS OF TROPOSPHERIC OZONE EXPOSURE: Reconciling Science and Standard Setting in the United States, Europe, and Asia , 2001 .

[30]  F. Woodward,et al.  Global response of terrestrial ecosystem structure and function to CO2 and climate change: results from six dynamic global vegetation models , 2001 .

[31]  P. Curtis,et al.  Elevated atmospheric CO2 and feedback between carbon and nitrogen cycles , 1993, Plant and Soil.

[32]  P. Reich,et al.  Quantifying plant response to ozone: a unifying theory. , 1987, Tree physiology.

[33]  Peter M. Vitousek,et al.  Ecosystem Succession and Nutrient Retention: A Hypothesis , 1975 .

[34]  B. Hungate,et al.  Priming depletes soil carbon and releases nitrogen in a scrub-oak ecosystem exposed to elevated CO2 , 2009 .

[35]  Yiqi Luo,et al.  Elevated CO2 stimulates net accumulations of carbon and nitrogen in land ecosystems: a meta-analysis. , 2006, Ecology.

[36]  Dale W. Johnson Progressive N limitation in forests: review and implications for long-term responses to elevated CO2. , 2006, Ecology.

[37]  R. E. Dickson,et al.  Forest atmosphere carbon transfer and storage (FACTS-II) the aspen Free-air CO2 and O3 Enrichment (FACE) project: an overview. , 2000 .

[38]  Michael G. Ryan,et al.  Age-Related Decline in Forest Productivity: Pattern and Process , 1997 .