Abstract
To study how grazing affects the uptake of inorganic and organic N forms, three focal plant species (i.e., the graminoid species Kobresia pygmaea, which decreases with grazing, and the forbs Potentilla bifurca and Potentilla multifida, which increase with grazing) were selected in ungrazed and grazed plots in an alpine meadow on the Tibetan Plateau. Three times during the growing season (i.e., June, July, and September), these plots were injected with 15N-labeled NO3 −-N, NH4 +-N, or glycine-N, or with only water as a control. Two hours after 15N injection, exchangeable NH4 +-N, glycine-N, and NO3 −-N as well as plant and soil samples were collected and analyzed for 15N/14N and total N content. Our result showed that all three plant species took up glycine-N, but uptake of inorganic N was generally predominant. The graminoid K. pygmaea took up all three N forms equally in June but preferred NO3 −-N in July (particularly under grazing) and exchangeable NH4 +-N in September. The forbs P. bifurca and P. multifida preferentially took up exchangeable NH4 +-N in July (particularly under grazing), while NO3 −-N was the dominant form of N uptake in September. P. bifurca generally preferred exchangeable NH4 +-N, but preference shifted toward NO3 −-N under grazing in June. P. multifida preferred glycine-N in ungrazed plots and shifted its preference to NO3 −-N under grazing in June. In conclusion, the three plant species showed niche partitioning for uptake of three forms of N across the season, which was modified by grazing. These findings indicate that plant N uptake patterns should be considered for better understanding the mechanisms of grazing effects on plant diversity and species coexistence.
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References
Andersen KM, Turner BL (2013) Preferences or plasticity in nitrogen acquisition by understorey palms in a tropical montane forest. J Ecol 101:819–825
Ashton IW, Miller AE, Bowman WD, Suding KN (2010) Niche complementarity due to plasticity in resource use: plant partitioning of chemical N forms. Ecology 91:3252–3260
Averill C, Finzi AC (2011) Increasing plant use of organic nitrogen with elevation is reflected in nitrogen uptake rates and ecosystem delta N15. Ecology 92:883–891
Bardgett RD, Streeter TC, Bol R (2003) Soil microbes compete effectively with plants for organic-nitrogen inputs to temperate grasslands. Ecology 84:1277–1287
Blagodatskaya B, Littschwager J, Lauerer M, Kuzyakov Y (2014) Plant traits regulating N capture define microbial competition in the rhizosphere. Eur J Soil Biol 61:41–48
Britto DT, Kronzucker HJ (2013) Ecological significance and complexity of N-source preference in plants. Ann Bot 112:957–963
Chapin FS, Moilanen L, Kielland K (1993) Preferential use of organic nitrogen for growth by a non-mycorrhizal arctic sedge. Nature 361:150–153
Chen H, Zhu Q, Peng C, Wu N, Wang Y, Fang X, Gao Y, Zhu D, Yang G, Tian J, Kang X, Piao S, Ouyang H, Xiang W, Luo Z, Jiang H, Song X, Zhang YG, Zhao X, Gong P, Yao T, Wu J (2013) The impacts of climate change and human activities on biogeochemical cycles on the Qinghai-Tibetan Plateau. Glob Chang Biol 19:2940–2955
Dorji T, Totland O, Moe SR, Hopping KA, Pan JB, Klein JA (2013) Plant functional traits mediate reproductive phenology and success in response to experimental warming and snow addition in Tibet. Glob Chang Biol 19:459–472
Eviner VT, Firestone MK (2007) Mechanisms determining patterns of nutrient dynamics. In: Stromberg MR, Corbin JD, D’Antonio CM (eds) California Grasslands:ecology and management. University of California Press, California, pp 94–106
Gao JQ, Mo Y, Xu XL, Zhang XW, Yu FH (2014) Spatiotemporal variations affect uptake of inorganic and organic nitrogen by dominant plant species in an alpine wetland. Plant Soil 381:271–278
Hafner S, Unteregelsbacher S, Seeber E, Lena B, Xu X, Li X, Guggenberger G, Miehe G, Kuzyakov Y (2012) Effect of grazing on carbon stocks and assimilate partitioning in a Tibetan montane pasture revealed by 13CO2 pulse labeling. Glob Chang Biol 18:528–538
Harrison KA, Bardgett RD (2004) Browsing by red deer negatively impacts on soil nitrogen availability in regenerating native forest. Soil Biol Biochem 36:115–126
Harrison KA, Bol R, Bardgett RD (2008) Do plant species with different growth strategies vary in their ability to compete with soil microbes for chemical forms of nitrogen? Soil Biol Biochem 40:228–237
Holst J, Liu CY, Bruggemann N, Butterbach-Bahl K, Zheng XH, Wang YS, Han SH, Yao ZS, Yue J, Han XG (2007) Microbial N turnover and N-oxide (N2O/NO/NO2) fluxes in semi-arid grassland of Inner Mongolia. Ecosystems 10:623–634
Jaeger CH, Monson RK, Fisk MC, Schmidt SK (1999) Seasonal partitioning of nitrogen by plants and soil microorganisms in an alpine ecosystem. Ecology 80:1883–1891
Jiang LL, Han XG, Dong N, Wang YF, Kardol P (2011) Plant species effects on soil carbon and nitrogen dynamics in a temperate steppe of northern China. Plant Soil 346:331–347
Jones DL, Shannon D, Murphy DV, Farrar J (2004) Role of dissolved organic nitrogen (DON) in soil N cycling in grassland soils. Soil Biol Biochem 36:749–756
Jones DL, Healey JR, Willett VB, Farrar JF, Hodge A (2005) Dissolved organic nitrogen uptake by plants - an important N uptake pathway? Soil Biol Biochem 37:413–423
Klein JA, Harte J, Zhao XQ (2007) Experimental warming, not grazing, decreases rangeland quality on the Tibetan Plateau. Ecol Appl 17:541–557
Kudoyarova GR, Dodd IC, Veselov DS, Rothwell SA, Veselov SY (2015) Common and specific responses to availability of mineral nutrients and water. J Exp Bot 66:2133–2144
Kuzyakov Y, Xu X (2013) Competition between roots and microorganisms for nitrogen: mechanisms and ecological relevance. New Phytol 198:656–669
LeBauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89:371–379
Li K, Liu X, Song L, Gong Y, Lu C, Yue P, Tian C, Zhang F (2015) Response of alpine grassland to elevated nitrogen deposition and water supply in China. Oecologia 177:65–72
Lovell RD, Jarvis SC, Bardgett RD (1995) Soil microbial biomass and activity in long-term grassland - effects of management changes. Soil Biol Biochem 27:969–975
Månsson KF, Olsson MO, Falkengren GU, Bengtsson G (2014) Soil moisture variations affect short-term plant-microbial competition for ammonium, glycine, and glutamate. Ecol Evol 4:1061–1072
Mcfarland JW, Ruess RW, Kielland K, Pregitzer K, Hendrick R (2010) Glycine mineralization in situ closely correlates with soil carbon availability across six North American forest ecosystems. Biogeochemistry 99:175–191
McKane RB, Johnson LC, Shaver GR, Nadelhoffer KJ, Rastetter EB, Fry B, Giblin AE, Kielland K, Kwiatkowski BL, Laundre JA (2002) Resource-based niches provide a basis for plant species diversity and dominance in arctic tundra. Nature 415:68–71
Mcnaughton SJ (1986) On Plants and Herbivores. Am Nat 128:765–770
Miller AE, Bowman WD (2003) Alpine plants show species-level differences in the uptake of organic and inorganic nitrogen. Plant Soil 250:283–292
Miller AE, Bowman WD, Suding KN (2007) Plant uptake of inorganic and organic nitrogen: neighbor identity matters. Ecology 88:1832–1840
Miller AE, Schimel JP, Sickman JO, Skeen KM, Melack T, Met J (2009) Seasonal variation in nitrogen uptake and turnover in two high-elevation soils: mineralization responses are site-dependent. Biogeochemistry 93:253–270
Nacry P, Bouguyon E, Gojon A (2013) Nitrogen acquisition by roots: physiological and developmental mechanisms ensuring plant adaptation to a fluctuating resource. Plant Soil 370:1–29
Nasholm T, Sandberg G, Ericsson A (1987) Quantitative-analysis of amino-acids in conifer tissues by high-performance liquid-chromatography and fluorescence detection of their 9-fluorenylmethyl chloroformate derivatives. J Chromatogr 396:225–236
Näsholm T, Kielland K, Ganeteg U (2009) Uptake of organic nitrogen by plants. New Phytol 182:31–48
Nelson D, Sommers L (1982) Dry combustion method using medium temperature resistance furnace. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis. Part 2. Chemical and microbial properties, 2nd edn. Soil Science Society of America and American Society of Agronomy Book Series no. 9, Madison, pp 539–579
Olofsson J, Kitti H, Rautiainen P, Stark S, Oksanen L (2001) Effects of summer grazing by reindeer on composition of vegetation, productivity and nitrogen cycling. Ecography 24:13–24
Pathan S, Ceccherini M, Hansen M, Giagnoni L, Ascher J, Arenella M, Sørensen S, Pietramellara G, Nannipieri P, Renella G (2015a) Maize lines with different nitrogen use efficiency select bacterial communities with different β-glucosidase-encoding genes and glucosidase activity in the rhizosphere. Biol Fertil Soils. doi:10.1007%2Fs00374-015-1045-9
Pathan SI, Ceccherini MT, Pietramellara G, Puschenreiter M, Giagnoni L, Arenella M, Varanini Z, Nannpieri P, Renella G (2015b) Enzyme activity and microbial community structure in the rhizosphere of two maize lines differing in N use efficiency. Plant Soil 387:413–424
Piao S, Fang J, He J (2006) Variations in Vegetation Net Primary Production in the Qinghai-Xizang Plateau, China, from 1982 to 1999. Clim Chang 74:253–267
Rui YC, Wang SP, Xu ZH, Wang YF, Chen CR, Zhou XQ, Kang XM, Lu SB, Hu YG, Lin QY, Luo CY (2011) Warming and grazing affect soil labile carbon and nitrogen pools differently in an alpine meadow of the Qinghai-Tibet Plateau in China. J Soil Sediment 11:903–914
Schimel JP, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecology 85:591–602
Schmidt S, Stewart GR (1999) Glycine metabolism by plant roots and its occurrence in Australian plant communities. Aust J Plant Physiol 26:253–264
Shen M, Tang Y, Chen J, Zhu X, Zheng Y (2011) Influences of temperature and precipitation before the growing season on spring phenology in grasslands of the central and eastern Qinghai-Tibetan Plateau. Agr Forest Meteorol 151:1711–1722
Streeter TC, Bol R, Bardgett RD (2000) Amino acids as a nitrogen source in temperate upland grasslands: the use of dual labelled (C-13, N-15) glycine to test for direct uptake by dominant grasses. Rapid Commun Mass Sp 14:1351–1355
Unteregelsbacher S, Hafner S, Guggenberger G, Miehe G, Xu X, Liu J, Kuzyakov Y (2012) Response of long-, medium-and short-term processes of the carbon budget to overgrazing-induced crusts in the Tibetan Plateau. Biogeochemistry 111:187–201
Vinolas LC, Vallejo VR, Jones DL (2001) Control of amino acid mineralization and microbial metabolism by temperature. Soil Biol Biochem 33:1137–1140
Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13:87–115
Wang WY, Wang QJ, Wang HC (2006) The effect of land management on plant community composition, species diversity, and productivity of alpine Kobersia steppe meadow. Ecol Res 21:181–187
Wang SP, Duan JC, Xu GP, Wang YF, Zhang Z, Rui YC, Luo CY, Xu B, Zhu XX, Chang XF (2012) Effects of warming and grazing on soil N availability, species composition, and ANPP in an alpine meadow. Ecology 93:2365–2376
Wang YJ, Wei XY, Yang P (2005) Effects of over-grazing on vegetation degradation of Kobresia pygmaea meadow in Nagqu, Tibet. J Lanzhou Univ Nat Sci 41:32–38
Warren CR (2014) Organic N molecules in the soil solution: what is known, what is unknown and the path forwards. Plant Soil 375:1–19
Wiener G, Jianlin H, Ruijun L (2003) The yak. FAO Regional Office for Asia and the Pacific. pp 28-47
Xu XL, Hua OY, Cao GM, Pei ZY, Zhou CP (2004) Uptake of organic nitrogen by eight dominant plant species in Kobresia meadows. Nutr Cycl Agroecosys 69:5–10
Xu XL, Ouyang H, Kuzyakov Y, Richter A, Wanek W (2006) Significance of organic nitrogen acquisition for dominant plant species in an alpine meadow on the Tibet plateau, China. Plant Soil 285:221–231
Xu XL, Ouyang H, Cao GM, Richter A, Wanek W, Kuzyakov Y (2011a) Dominant plant species shift their nitrogen uptake patterns in response to nutrient enrichment caused by a fungal fairy in an alpine meadow. Plant Soil 341:495–504
Xu XL, Ouyang H, Richter A, Wanek W, Cao GM, Kuzyakov Y (2011b) Spatio-temporal variations determine plant-microbe competition for inorganic nitrogen in an alpine meadow. J Ecol 99:563–571
Yan L, Zhou GS, Zhang F (2013) Effects of different grazing intensities on grassland production in China: a meta-analysis. PLoS One 8, e81466
Yang HJ, Li Y, Wu MY, Zhang Z, Li LH, Wan SQ (2011) Plant community responses to nitrogen addition and increased precipitation: the importance of water availability and species traits. Glob Chang Biol 17:2936–2944
Zheng SX, Lan ZC, Li WH, Shao RX, Shan YM, Wan HW, Taube F, Bai YF (2011) Differential responses of plant functional trait to grazing between two contrasting dominant C3 and C4 species in a typical steppe of Inner Mongolia, China. Plant Soil 340:141–155
Zhou XM (2001) Alpine Kobresia meadows in China. Science Press, Beijing, pp 51–62
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This work was supported by funding from the National Science Foundation of China (41230750, 41301600), the National Basic Research Program (2013CB956000), and the Strategic Priority Research Program (B) of the Chinese Academy of Sciences (XDB03030403).
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Jiang, L., Wang, S., Pang, Z. et al. Grazing modifies inorganic and organic nitrogen uptake by coexisting plant species in alpine grassland. Biol Fertil Soils 52, 211–221 (2016). https://doi.org/10.1007/s00374-015-1069-1
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DOI: https://doi.org/10.1007/s00374-015-1069-1