Does N limit C sequestration in terrestrial ecosystems? If so, how? Yiqi Luo Department of Botany and Microbiology University of Oklahoma USA

Key points 1. 1.Mineral N regulates plant growth and its responses to global change 2. 2.N capital in organic form determines long-term carbon sequestration

Working hypotheses 1.CO 2 stimulation of carbon sequestration will be down-regulated by limited N supply over time. 2.Climate warming stimulates N mineralization and increases N availability, which will enhance C sequestration 3.N deposition increases mineral N availability, stimulate plant growth, and thus will enhance C sequestration

Carbon cycle Soil Mineral N Nitrogen cycle Plant assimilation Warming N deposition Elevated CO 2

Effects of nitrogen on plant growth, overall and grouped by biome LeBauer and Treseder 2008

Plant Carbon cycle Soil Mineral N Nitrogen cycle assimilation Atm CO 2 Litter / CWD Soil Organic Matter N deposition N fixation denitrification N leaching respiration Internal fast External slow mineralization photosynthesis litterfall & mortality decomposition (i) Thornton et al. 2009

Effects of N addition on C and N cycles Meta-analysis of data from 206 papers Lu et al New Phytologist (N cycle) Lu et al Agricultural Ecosystems & Environment (C cycle)

Leaching 461% N 2 O 134%Den 84% N addition NH % N uptake NO % Aboveground plant N 44% Belowground plant N 53% N-Min 25% Litter/OH decomposition Litter N 24% Organic Horizon N 6.1% Soil N pool 6.2% Microbial biomass N 5.8% DON 21% Nit. 154% Extremely leaking system Lu et al. 2011a

O’Sullivan et al GCB Once N fertilization stops, mineral N gradually reset to the control level

N additions Aboveground plant C 35.7% Ps Belowground plant C 23% Litter/OH decomposition Litter C 20.9% Organic Horizon C 1.8% Deep layer SOM DOC 11% R:S 14.5 Rs 4.3% Soil organic C 2.2% Microbe C 6.4% 1.Reduce C input into soil systems 2.Little contributions of aboveground biomass and litter production to soil C 3.Increased C loss via decomposition and respiration 4.Increased C loss via DOC Lu et al. 2011b

Mack et al Nature

Mineral N does not set the level of soil N capital over time

“dummy” heater Infrared heater clip unclip clip Long-term (12 years) warming and clipping

C and N interactions under experimental warming Plant community C 4 /C 3 species Leaf Ps Phenology Growing season Plant growth Microbial community Fungi/bacteria Plant N uptake Plant & soil C Available N Quality of bulk litter Respiration NUE Litter Decomposition Luo, Ann. Rev. Ecol. Evol. System

Plant community C 4 /C 3 species Leaf Ps Phenology Growing season Plant growth Microbial community Fungi/bacteria Plant N uptake Plant & soil C Available N Quality of bulk litter Respiration NUE Litter Decomposition Sherry et al. 2007, PNAS Zhou et al. 2007a, JIPB Zhou et al. 2006, GBC; 2007b, GCB Luo et al. 2001, Nature Zhang et al GCB Zhou et al. In review An et al. 2005, GCB Cheng et al Agric Ecosystems Wan et al. 2005, GBC Luo et al. 2009, GCB-E Sherry et al. 2008, GCB Niu et al. 2010, Ecology

Niu et al Ecology NUE is the main mechanism underlying warming- induced increases in plant C storage

Lu et al. In preparation

Warming effects on carbon processes Lu et al. In preparation

NPP N sequestered in biomass & litter C input to soil N sequestered in SOM labile soil N N uptake N availability C:N CO 2 P rogressive N itrogen L imitation Luo et al BioScineces

NPP N sequestered in biomass & litter C input to soil N sequestered in SOM labile soil N N uptake N availability C:N CO 2 Luo et al BioScineces PNL may not occur if N fixation N loss

Luo et al Ecology 21% increase in litter C 25% increase in litter N 5.6% increase in soil C 11.2% increase in soil N Ecosystem C increases by ~100 g m -2 yr -1 Ecosystem N increases by ~1 g m -2 yr -1 No complete down-regulation

Working hypotheses N capital increased by ~1 g N m -1 yr -1 to alleviate N limitation Increased N mineralization enhances biomass growth but not soil C sequestration. Yes for plant pools, not for soil pools CO 2 stimulation of carbon sequestration will be down- regulated by limited N supply over time. Climate warming stimulates N mineralization and increases N availability, which will enhance C sequestration N deposition increases mineral N availability, stimulate plant growth, and thus will enhance C sequestration

Soil mineral N availability regulates plant growth but does not determine long-term C sequestration Which N processes determine long- term C sequestration?

Rastteter et al. 1997

N capital in organic form  Long-term C sequestration Redistribution of N among pools  intermediate C sequestration Adjustment in C/N ratio  short- term C sequestration Rastteter et al. 1997

Binkley et al Ecosystems N capital

Adding inorganic N Lu et al. 2011, New Phytologist Fire Wan et al. 2001, Ecological Appl Plant invasionLiao et al. 2008, New Phytologist Forest successionYang et al. 2011, New Phytologist Forest plantationLiao et al. 2010, PloS One Elevated CO 2 Luo et al. 2006, Ecology Experimental warmingLu et al. In preparation Net change in organic N capital (the key variable to determine long-term C sequestration)

A database of 124 published papers from the literature Carbon and nitrogen coupling during forest succession Yang et al New Phytologists

The rates of C pool changes declined with forest age and approached an equilibrium state

Yang et al New Phytologists The rate of relative N change was positively associated with the rate of relative C change with different slopes among various ecosystem components

Yang et al New Phytologists The rate of absolute N change increased linearly with that of C pool change

Yang et al. Unpublished

Yang et al New Phytologists The relative change in C: N ratio was larger than 1.0 in both aboveground plant and woody tissues, but close to 1.0 in other ecosystem components

Conclusions 1. 1.Mineral N limits plant growth but does not regulate long-term carbon sequestration 2. 2.Organic N capital determines long-term carbon sequestration

Acknowledgement Financial support: U.S. National Science Foundation US Department of Energy NCEAS Working group: William Currie, Jeffrey Dukes, Christopher Field,,Adrien Finzi, Ueli Hartwig, Bruce Hungate, Yiqi Luo, Ross McMurtrie, Ram Oren, William Parton, Diane Pataki, Rebecca Shaw, Bo Su, Donald Zak Meta analysis collaborators: Dafeng Hui, Chengzhang Liao, Meng Lu, Shuli Niu, Shiqiang Wan, Yuanhe Yang, Deqiang Zhang, Xuhui Zhou