Abstract
The effects of global change factors on the stoichiometric composition of green and senesced plant tissues are critical determinants of ecosystem feedbacks to anthropogenic-driven global change. So far, little is known about species stoichiometric responses to these changes. We conducted a manipulative field experiment with nitrogen (N; 17.5 g m−2 year−1) and water addition (180 mm per growing season) in a temperate steppe of northern China that is potentially highly vulnerable to global change. A unique and important outcome of our study is that water availability modulated plant nutritional and stoichiometric responses to increased N availability. N addition significantly reduced C:N ratios and increased N:P ratios but only under ambient water conditions. Under increased water supply, N addition had no effect on C:N ratios in green and senesced leaves and N:P ratios in senesced leaves, and significantly decreased C:P ratios in both green and senesced leaves and N:P ratios in green leaves. Stoichiometric ratios varied greatly among species. Our results suggest that N and water addition and species identity can affect stoichiometric ratios of both green and senesced tissues through direct and interactive means. Our findings highlight the importance of water availability in modulating stoichiometric responses of plants to potentially increased N availability in semi-arid grasslands.
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References
Aerts R, Callaghan TV, Dorrepaal E, van Logtestijn R, Cornelissen JHC (2009) Seasonal climate manipulations result in species-specific changes in leaf nutrient levels and isotopic composition in a sub-arcitc bog. Funct Ecol 23:680–688
Aerts R, Chapin FS III (2000) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Adv Ecol Res 30:1–67
Augustine DJ, McNaughton SJ, Frank DA (2003) Feedbacks between soil nutrients and large herbivores in a managed savanna ecosystem. Ecol Appl 13:1325–1337
Bai YF, Han XG, Wu JG, Chen ZZ, Li LH (2004) Ecosystem stability and compensatory effects in the Inner Mongolia grassland. Nature 431:181–184
Bai YF, Wu JG, Clark CM, Naeem S, Pan QM, Huang JH, Zhang LX, Han XG (2010) Tradeoffs and thresholds in the effects of nitrogen addition on biodiversity and ecosystem functioning: evidence from Inner Mongolia grasslands. Glob Change Biol 16:358–372
Bai YF, Wu JG, Xing Q, Pan QM, Huang JH, Yang DL, Han XG (2008) Primary production and rain use efficiency across a precipitation gradient on the Mongolia plateau. Ecology 89:2140–2153
Billings SA, Zitzer SF, Weatherly H, Schaeffer SM, Charlet T, Arnone JA, Evans RD (2003) Effects of elevated carbon dioxide on green leaf tissue and leaf litter quality in an intact Mojave Desert ecosystem. Glob Change Biol 9:729–735
Christensen L, Coughenour MB, Ellis JE, Chen ZZ (2004) Vulnerability of the Asian typical steppe to grazing and climate change. Clim Change 63:351–368
Clark CM, Tilman D (2008) Loss of plant species after chronic low-level nitrogen deposition to prairie grasslands. Nature 451:712–715
Ding YH, Ren GY, Zhao ZC, Xu Y, Luo Y, Li QP, Zhang J (2007) Detection, causes and projection of climate change over China: an overview of recent progress. Adv Atmos Sci 249:954–971
Dukes JS, Chiariello NR, Cleland EE, Moore LA, Shaw MR, Thayer S, Tobeck T, Mooney HA, Field CB (2005) Responses of grassland production to single and multiple global environmental changes. PLoS Biol 3:1829–1837
Elser JJ, Fagan WF, Denno RF, Dobberfuhl DR, Folarin A, Huberty A, Interlandi S, Kilham SS, McCauley E, Schulz KL, Siemann EH, Sterner RW (2000) Nutritional constraints in terrestrial and freshwater food webs. Nature 408:578–580
Esmeijer-Liu A, Aerts R, Kurschner W, Bobbink R, Lotter A, Verhoeven J (2009) Nitrogen enrichment lowers Betula pendula green and yellow leaf stoichiometry irrespective of effects of elevated carbon dioxide. Plant Soil 316:311–322
Fujita Y, Robroek BJM, de Ruiter PC, Heil GW, Wassen MJ (2010) Increased N affects P uptake of eight grassland species: the role of root surface phosphatase activity. Oikos 119:1665–1673
Galloway JN, Cowling EB (2002) Reactive nitrogen and the world: 200 years of change. Ambio 31:64–71
Galloway JN, Dentener FJ, Capone DG, Boyer EW, Howarth RW, Seitzinger SP, Asner GP, Cleveland C, Green P, Holland E, Karl DM, Michaels AF, Porter JH, Townsend A, Vörösmarty C (2004) Nitrogen cycles: past, present and future. Biogeochemistry 70:153–226
Gerten D, Luo Y, Le Maire G, Parton WJ, Keough C, Weng E, Beier C, Ciais P, Cramer W, Dukes JS, Hanson PJ, Knapp AAK, Linder S, Nepstad D, Rustad L, Sowerby A (2008) Modelled effects of precipitation on ecosystem carbon and water dynamics in different climatic zones. Glob Change Biol 14:2365–2379
Gruber N, Galloway JN (2008) An Earth-system perspective of the global nitrogen cycle. Nature 451:293–298
Güsewell S (2004) N:P ratios in terrestrial plants: variation and functional significance. New Phytol 164:243–266
Güsewell S (2005) Responses of wetland graminoids to the relative supply of nitrogen and phosphorus. Plant Ecol 176:35–55
Güsewell S, Gessner MO (2009) N:P ratios influence litter decomposition and colonization by fungi and bacteria in microcosms. Funct Ecol 23:211–219
Güsewell S, Koerselman W, Verhoeven JTA (2002) Time-dependent effects of fertilization on plant biomass in floating fens. J Veg Sci 13:705–718
Harpole WS, Potts DL, Suding KN (2007) Ecosystem responses to water and nitrogen amendment in a California grassland. Glob Change Biol 13:2341–2348
He JS, Fang JY, Wang ZH, Guo DL, Flynn DFB, Geng Z (2006) Stoichiometry and large-scale patterns of leaf carbon and nitrogen in the grassland biomes of China. Oecologia 149:115–122
He JS, Wang L, Flynn DFB, Wang XP, Ma WH, Fang JY (2008) Leaf nitrogen:phosphorus stoichiometry across Chinese grassland biomes. Oecologia 155:301–310
Heisler-White JL, Knapp AK, Kelly EF (2008) Increasing precipitation event size increases aboveground net primary productivity in a semi-arid grassland. Oecologia 158:129–140
Henry HAL, Chiariello NR, Vitousek PM, Mooney HA, Field CB (2006) Interactive effects of fire, elevated carbon dioxide, nitrogen deposition, and precipitation on a California annual grassland. Ecosystems 9:1066–1075
Henry HAL, Cleland EE, Field CB, Vitousek PM (2005) Interactive effects of elevated CO2, N deposition and climate change on plant litter quality in a California annual grassland. Oecologia 142:465–473
Hobbie SE (2005) Contrasting effects of substrate and fertilizer nitrogen on the early stages of litter decomposition. Ecosystems 8:644–656
Hooper DU, Johnson L (1999) Nitrogen limitation in dryland ecosystems: Responses to geographical and temporal variation in precipitation. Biogeochemistry 46:247–293
Huxman TE, Snyder KA, Tissue D, Leffler AJ, Ogle K, Pockman WT, Sandquist DR, Potts DL, Schwinning S (2004) Precipitation pulses and carbon fluxes in semiarid and arid ecosystems. Oecologia 141:254–268
Kerkhoff AJ, Fagan WF, Elser JJ, Enquist BJ (2006) Phylogenetic and growth form variation in the scaling of nitrogen and phosphorus in the seed plants. Am Nat 168:E103–E122
Knapp AK, Burns CE, Fynn RWS, Kirkman KP, Morris CD, Smith MD (2006) Convergence and contingency in production-precipitation relationships in North American and South African C-4 grasslands. Oecologia 149:456–464
Knapp AK, Fay PA, Blair JM, Collins SL, Smith MD, Carlisle JD, Harper CW, Danner BT, Lett MS, Mccarron JK (2002) Rainfall variability, carbon cycling, and plant species diversity in a mesic grassland. Science 298:2202–2205
Knops JMH, Naeem S, Reich PB (2007) The impact of elevated CO2, increased nitrogen availability and biodiversity on plant tissue quality and decomposition. Glob Change Biol 13:1960–1971
Knops JMH, Wedin D, Tilman D (2001) Biodiversity and decomposition in experimental grassland ecosystems. Oecologia 126:429–433
Kobe RK, Lepczyk CA, Iyer M (2005) Resorption efficiency decreases with increasing green leaf nutrients in a global data set. Ecology 86:2780–2792
Koerselman W, Meuleman AFM (1996) The vegetation N:P ratio: a new tool to detect the nature of nutrient limitation. J Appl Ecol 33:1441–1450
Kozovits AR, Bustamante MMC, Garofalo CR, Bucci S, Franco AC, Goldstein G, Meinzer FC (2007) Nutrient resorption and patterns of litter production and decomposition in a Neotropical Savanna. Funct Ecol 21:1034–1043
Liu P, Huang JH, Han XG, Sun OJ, Zhou Z (2006) Differential responses of litter decomposition to increased soil nutrients and water between two contrasting grassland plant species of Inner Mongolia, China. Appl Soil Ecol 34:266–275
Lü XT, Han XG (2010) Nutrient resorption responses to water and nitrogen amendment in semi-arid grassland of Inner Mongolia, China. Plant Soil 327:481–491
Manzoni S, Jackson RB, Trofymow JA, Porporato A (2008) The global stoichiometry of litter nitrogen mineralization. Science 321:684–686
Menge DNL, Field CB (2007) Simulated global changes alter phosphorus demand in annual grassland. Glob Change Biol 13:2582–2591
Novotny AM, Schade JD, Hobbie SE, Kay AD, Kyle M, Reich PB, Elser JJ (2007) Stoichiometric response of nitrogen-fixing and non-fixing dicots to manipulations of CO2, nitrogen, and diversity. Oecologia 151:687–696
Olsen SR, Cole CV, Watanabe FS, Dean LA (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. Circular No. 939. USDA
Patrick L, Cable J, Potts D, Ignace D, Barron-Gafford G, Griffith A, Alpert H, Van Gestel N, Robertson T, Huxman TE, Zak J, Loik ME, Tissue D (2007) Effects of an increase in summer precipitation on leaf, soil, and ecosystem fluxes of CO2 and H2O in a sotol grassland in Big Bend National Park, Texas. Oecologia 151:704–718
Penuelas J, Rutishauser T, Filella I (2009) Phenology feedbacks on climate change. Science 325:887–888
Perring MP, Hedin LO, Levin SA, McGroddy M, De Mazancourt C (2008) Increased plant growth from nitrogen addition should conserve phosphorus in terrestrial ecosystems. Proc Natl Acad Sci USA 105:1971–1976
Phoenix GK, Booth RE, Leake JR, Read DJ, Grime JP, Lee JA (2003) Simulated pollutant nitrogen deposition increases P demand and enhances root-surface phosphatase activities of three plant functional types in a calcareous grassland. New Phytol 161:279–289
Pugnaire FI (2001) Variability of inorganic nutrient concentrations in leaves. New Phytol 150:506–507
Schade JD, Kyle M, Hobbie SE, Fagan WF, Elser JJ (2003) Stoichiometric tracking of soil nutrients by a desert insect herbivore. Ecol Lett 6:96–101
Sterner RW, Elser JJ (2002) Ecological stoichiometry. Princeton University Press, Princeton
Suttle KB, Thomsen MA, Power ME (2007) Species interactions reverse grassland responses to changing climate. Science 315:640–642
Vitousek PM, Mooney HA, Lubchenco J, Melillo JM (1997) Human domination of Earth’s ecosystems. Science 277:494–499
Wang CH, Wan SQ, Xing XR, Zhang L, Han XG (2006) Temperature and soil moisture interactively affected soil net N mineralization in temperate grassland in Northern China. Soil Biol Biochem 38:1101–1110
Weltzin JF, Loik ME, Schwinning S, Williams DG, Fay PA, Haddad BM, Harte J, Huxman TE, Knapp AK, Lin GH, Pockman WT, Shaw MR, Small EE, Smith MD, Smith SD, Tissue DT, Zak JC (2003) Assessing the response of terrestrial ecosystems to potential changes in precipitation. Bioscience 53:941–952
Xia JY, Wan SQ (2008) Global response patterns of terrestrial plant species to nitrogen addition. New Phytol 179:428–439
Zavaleta ES, Shaw MR, Chiariello NR, Thomas BD, Cleland EE, Field CB, Mooney HA (2003) Grassland responses to three years of elevated temperature, CO2, precipitation, and N deposition. Ecol Monogr 73:585–604
Zhang LX, Bai YF, Han XG (2004) Differential responses of N:P stoichiometry of Leymus chinensis and Carex korshinskyi to N additions in a steppe ecosystem in Nei Mongol. Acta Bot Sinica 46:259–270
Acknowledgments
We thank the staff of the Inner Mongolia Grassland Ecosystem Research Station (IMGERS) for facilitating this study. We gratefully acknowledge Weijun Wu, Yongsheng Jin and Qiang Li for field and laboratory assistance. We also wish to thank Andrea Polle and three anonymous reviewers who provided valuable comments and suggestions. This work was supported by The Knowledge Innovation Project of CAS (No. KZCX2-YW-T06), the Ministry of Science and Technology (2007CB106801), and the National Natural Science Foundation of China (30830026 and 30821062).
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Communicated by Andrea Polle.
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Lü, XT., Kong, DL., Pan, QM. et al. Nitrogen and water availability interact to affect leaf stoichiometry in a semi-arid grassland. Oecologia 168, 301–310 (2012). https://doi.org/10.1007/s00442-011-2097-7
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DOI: https://doi.org/10.1007/s00442-011-2097-7