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Effects of grazing on the acquisition of nitrogen by plants and microorganisms in an alpine grassland on the Tibetan plateau

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Abstract

Background and aims

Nitrogen (N) limitation leads to intense competition between plants and soil microorganisms for available N. However, it is unclear how grazing affects the acquisition of N by plants and microorganisms.

Methods

We conducted short-term 15N tracer experiments during the growing season (June, early growing season; July, mid-growing season; and September, late growing season) in an alpine grassland on the Tibetan Plateau to investigate the effects of grazing on the acquisition of NO3 −-N, NH4 +-N, and glycine-N by plants and soil microorganisms. Three dominant plant species (one graminoid, Kobresia pygmaea, and two forbs, Potentilla bifurca and Potentilla multifida) were selected for the study. As these species represented >90% of the vegetation, the plant recovery of 15N reflected competition at the plant community.

Results

Grazing decreased the recovery of 15N by soil microorganisms and plants by 46 and 69%, respectively, indicating that grazing strongly reduced the uptake of 15N by plants and microorganisms and altered the partitioning of 15N between them. Significant interactions were found between grazing, season and the different forms of N. In the absence of grazing, plants acquired relatively more N than soil microorganisms for the three forms of N in July and September, whereas the microorganisms obtained relatively more 15N glycine in July and all three forms of N in September under grazing conditions. Under grazing, the plant root biomass played an important role in controlling plant–microbial N acquisition.

Conclusions

Grazing alters the partitioning of inorganic and organic N between plants and soil microorganisms by reducing microbial 15N recovery to a lesser extent than plant 15N recovery. This indicates that heterotrophic microorganisms play an important part in N cycling in N-limited ecosystems.

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References

  • Bardgett RD, Streeter TC, Bol R (2003) Soil microbes compete effectively with plants for organic nitrogen inputs to temperate grasslands. Ecology 84:1277–1287

    Article  Google Scholar 

  • Blagodatskaya E, Kuzyakov Y (2013) Active microorganisms in soil: critical review of estimation criteria and approaches. Soil Biol Biochem 67:192–211

    Article  CAS  Google Scholar 

  • Brookes PC, Landman A, Pruden G, Jenkinson DS (1985) Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem 17:837–842

    Article  CAS  Google Scholar 

  • Chapin FS, Moilanen L, Kielland K (1993) Preferential use of organic nitrogen for growth by a non-mycorrhizal arctic graminoids. Nature 361:150–153

    Article  CAS  Google Scholar 

  • Chen J, Carrillo Y, Pendall E, Dijkstra FA, Evans RD, Morgan JA, Williams DG (2015a) Soil microbes compete strongly with plants for soil inorganic and amino acid nitrogen in a semiarid grassland exposed to elevated CO2 and warming. Ecosystems 18:861–880

    Article  CAS  Google Scholar 

  • Chen J, Zelikova TJ, Pendall E, Morgan JA, Williams DG (2015b) Daily and seasonal changes in soil amino acid composition in a semiarid grassland exposed to elevated CO2 and warming. Biogeochemistry 123:135–146

    Article  CAS  Google Scholar 

  • Crenshaw CL, Lauber C, Sinsabaugh RL, Stavely LK (2008) Fungal control of nitrous oxide production in semiarid grassland. Biogeochemistry 87:17–27

    Article  CAS  Google Scholar 

  • de Vries F, Bardgett RD (2012) Plant-microbial linkages and ecosystem nitrogen retention: lessons for sustainable agriculture. Frontiers Ecol Environ 10:425–432

    Article  Google Scholar 

  • de Vries FT, Bardgett RD (2016) Plant community controls on shor-term ecosystem nitrogen retention. New Phytol 210:861–874

    Article  PubMed  PubMed Central  Google Scholar 

  • de Vries FT, Jørgensen HB, Hedlund K, Bardgett RD (2015) Disentangling plant and soil microbial controls on carbon and nitrogen loss in grassland mesocosms. J Ecol 103:629–640

    Article  Google Scholar 

  • Demoling F, Figueroa D, Bååth E (2007) Comparison of factors limiting bacterial growth in different soils. Soil Biol Biochem 39:2485–2495

    Article  CAS  Google Scholar 

  • Dijkstra FA, He MZ, Johan MP (2015) Plant and microbial uptake of nitrogen and phosphorus affected by drought using N-15 and P-32 tracers. Soil Biol Biochem 82:135–142

    Article  CAS  Google Scholar 

  • Farrell M, Hill PW, Farrar J, Bardgett RD, Jones DL (2011) Seasonal variation in soluble soil carbon and nitrogen across a grassland productivity gradient. Soil Biol Biochem 43:835–844

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Greenwood K, McKenzie B (2001) Grazing effects on soil physical properties and the consequences for pastures: a review. Anim Prod Sci 41:1231–1250

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Hill PW, Farrar J, Roberts P, Farrell M, Grant H, Newsham KK, Hopkins DW, Bardgett RD, Jones DL (2011) Vascular plant success in a warming Antarctic may be due to efficient nitrogen acquisition. Nat Clim Chang 1:50–53

    Article  CAS  Google Scholar 

  • Hobbie JE, Hobbie EA (2013) Microorganisms in nature are limited by carbon and energy: the starving-survival lifestyle in soil and consequences for estimating microbial rates. Front Microbiol 4:1–11

    Article  Google Scholar 

  • Hodge A, Robinson D, Fitter A (2000) Are microorganisms more effective than plants at competing for nitrogen? Trends Plant Sci 5:304–308

    Article  CAS  PubMed  Google Scholar 

  • Jaeger CH, Monson RK, Fisk MC, Schmidt SK (1999) Seasonal partitioning of nitrogen by plants and soil microbes in an alpine ecosystem. Ecology 80:1883–1891

    Article  Google Scholar 

  • Jiang LL, Wang SP, Pang Z, Wang CS, Kardol P, Zhou XQ, Rui YC, Lan ZC, Wang YF, Xu XL (2016) Grazing modifies inorganic and organic nitrogen uptake by coexisting plant species in alpine grassland. Biol Fert Soils 52:211–221

    Article  CAS  Google Scholar 

  • Jirout J, Simek M, Elhottova D (2013) Fungal contribution to nitrous oxide emissions from cattle impacted soils. Chemosphere 90:565–572

    Article  CAS  PubMed  Google Scholar 

  • Jonasson S, Michelsen A, Schmidt IK (1999) Responses in microbes and plants to changed temperature, nutrient, and light regimes in the arctic. Ecology 80:1828–1843

    Article  Google Scholar 

  • Jones DL, Hughes LT, Murphy DV, Healey JR (2008) Dissolved organic carbon and nitrogen dynamics in temperate coniferous forest plantations. Eur J Soil Sci 59:1038–1048

    Article  CAS  Google Scholar 

  • Kalbitz K, Solinger S, Park JH, Michalzik B, Matzner E (2000) Controls on the dynamics of dissolved organic matter in soils: a review. Soil Sci 165:277–304

    Article  CAS  Google Scholar 

  • Kaštovská E, Šantrůčková H (2011) Comparison of uptake of different N forms by soil microorganisms and two wet-grassland plants: a pot study. Soil Biol Biochem 43:1285–1291

    Article  Google Scholar 

  • Kaye JP, Hart SC (1997) Competition for nitrogen between plants and soil microorganisms. Trends Ecol Evol 12:139–143

    Article  CAS  PubMed  Google Scholar 

  • Kuster TM, Wilkinson A, Hill PW, Jones DL, Bardgett RD (2016) Warming alters competition for organic and inorganic nitrogen between co-existing grassland plant species. Plant Soil 406:117–129

    Article  CAS  Google Scholar 

  • Kuzyakov Y, Xu XL (2013) Competition between roots and microbes for nitrogen: mechanisms and ecological relevance. New Phytol 198:656–669

  • Liu QY, Qiao N, Xu XL (2016) Nitrogen acquisition by plants and microorganisms in a temperate grassland. Scientific Reports 6:22642

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Lu X, Kelsey KC, Yan Y, Sun J, Wang X, Cheng G, Neff CJ (2017) Effects of grazing on ecosystem structure and function of alpine grasslands in Qinghai–Tibetan Plateau: a synthesis. Ecosphere 8(1):e01656

  • Mansson KF, Olsson MO, Falkengren-Grerup U, Bengtsson G (2014) Soil moisture variations affect short-term plant-microbial competition for ammonium, glycine, and glutamate. Ecol Evol 4:1061–1072

    Article  PubMed  PubMed Central  Google Scholar 

  • Marusenko Y, Huber DP, Hall SJ (2013) Fungi mediate nitrous oxide production but not ammonia oxidation in aridland soils of the southwestern US. Soil Biol Biochem 63:24–36

    Article  CAS  Google Scholar 

  • McKane RB, Johnson LC, Shaver GR, Nadelhoffer KJ, Rastetter EB, Fry B, Giblin AE, Kielland K, Kwiatkowski BL, Laundre JA, Murray G (2002) Resource-based niches provide a basis for plant species diversity and dominance in arctic tundra. Nature 415:68–71

    Article  CAS  PubMed  Google Scholar 

  • Milchunas DG, Lauenroth WK (1993) Quantitative Effects of Grazing on Vegetation and Soils Over a Global Range of Environments. Ecol Monogr 63:327–366

  • Näsholm 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 Chromatog 396:225–236

    Article  Google Scholar 

  • Nelson D, Sommers L (1982) Dry combustion method using medium temperature resistance furnace. In: Page AL et al. (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.9:539–579

  • 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

    Article  CAS  Google Scholar 

  • Recous S, Mary B, Faurie G (1990) Microbial immobilization of ammonium and nitrate in cultivated soils. Soil Biol Biochem 22:913–922

    Article  CAS  Google Scholar 

  • 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 Soils Sediments 11:903–914

    Article  CAS  Google Scholar 

  • Saggar S, Bolan NS, Bhandral R, Hedley CB, Luo J (2004) A review of emissions of methane, ammonia, and nitrous oxide from animal excreta deposition and farm effluent application in grazed pastures. New Zealand J Agr Res 47:513–544

    Article  CAS  Google Scholar 

  • 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. Agric For Meteorol 151:1711–1722

    Article  Google Scholar 

  • Sistla S, Schimel J (2012) Stoichiometric flexibility as a regulator of carbon and nutrient cycling in terrestrial ecosystems under change. New Phytol 196:68–78

    Article  CAS  PubMed  Google Scholar 

  • Song MH, Xu XL, Hu QW, Tian YQ, Hua OY, Zhou CP (2007) Interactions of plant species mediated plant competition for inorganic nitrogen with soil microbesin an alpine meadow. Plant Soil 297:127–137

    Article  CAS  Google Scholar 

  • Tiedje JM (1982) Methods of Soil Analysis. Part 2. Chemical and Microbiological Properties (2nd Edn.), American Society of Agronomy and Soil Science Society of America, Madison, WI, 821–830

  • 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

    Article  Google Scholar 

  • Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13:87–115

    Article  Google Scholar 

  • 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

  • Wang ZP, Han XG, Li LH (2008) Effects of grassland conversion to croplands on soil organic carbon in the temperate Inner Mongolia. J Environ Manag 86:529–534

    Article  CAS  Google Scholar 

  • Wang S, Duan J, Xu G, Wang Y, Zhang Z, Rui Y, Luo C, Xu B, Zhu X, Chang X (2012) Effects of warming and grazing on soil N availability, species composition, and ANPP in an alpine meadow. Ecology 93:2365–2376

    Article  PubMed  Google Scholar 

  • Wiener G, Jianlin H, Ruijun L (2003) The yak. FAO Regional Office for Asia and the Pacific pp 28–47

  • Wu H, Dannenmann M, Fanselow N, Wolf B, Yao Z, Wu X, Brüggemann N, Zheng X, Han X, Dittert K (2011) Feedback of grazing on gross rates of N mineralization and inorganic N partitioning in steppe soils of Inner Mongolia. Plant Soil 340:127–139

    Article  CAS  Google Scholar 

  • Xu XL, Ouyang H, Pei ZY, Zhou CP (2003) The fate of short-term 15N labeled nitrate and ammonium added to an alpinemeadow in the Qinghai-Xizang plateau, China. Act Bot Sin 45:276–281

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Xu X, Ouyang H, Richter A, Wanek W, Cao G, Kuzyakov Y (2011a) Spatio-temporal variations determine plant-microbe competition for inorganic nitrogen in an alpine meadow. J Ecol 99:563–571

    CAS  Google Scholar 

  • Xu XL, Ouyang H, Cao GM, Richter A, Wanek W, Kuzyakov Y (2011b) 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

    Article  CAS  Google Scholar 

  • Xu XL, Wanek W, Zhou C, Richter A, Song M, Cao G, Ouyang H, Kuzyakov Y (2014) Nutrient limitation of alpine plants: implications from leaf N : P stoichiometry and leaf delta N-15. J Plant Nutr Soil Sci 177:378–387

    Article  CAS  Google Scholar 

  • Yan L, Zhou GS, Zhang F (2013) Effects of different grazing intensities on grassland production in China: a meta-analysis. PLoS One 8. doi:10.1371/journal.pone.0081466

  • Yang Y, Fang J, Fay AP, Bell JE, Ji C (2010) Rain use efficiency across a precipitation gradient on the Tibetan plateau. Geoph Res Let 37:L15702. doi:10.1029/2010GL043920

  • Yang YF, Wu L, Lin Q, Yuan M, Xu D, Yu H, Hu Y, Duan J, Li X, He Z (2013) Responses of the functional structure of soil microbial community to livestock grazing in the Tibetan alpine grassland. Glob Change Biol 19:637–648

    Article  Google Scholar 

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Acknowledgements

This work was supported by funding from the National Science Foundation of China (41230750), the National Basic Research Program (2013CB956000), the National Science Foundation of China (31672474), the National Key Research and Development Program of China (2016YFC0501802), the Strategic Priority Research Program (B) of the Chinese Academy of Sciences (XDB15010201) and the National Science Foundation of China (41301600 and 41671253). We thank Haishan Niu for helping with the data analysis.

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Authors and Affiliations

  1. Key Laboratory of Alpine Ecology and Biodiversity, Institute of Tibetan Plateau Research, Chinese Academy of Sciences, Beijing, 100101, China

    Lili Jiang & Shiping Wang

  2. Key Laboratory of Adaptation and Evolution of Plateau Biota, Northwest Institute of Plateau Biology, Chinese Academy of Sciences, Xining, 810008, China

    Caiyun Luo & Zhenhua Zhang

  3. CAS Center for Excellence in Tibetan Plateau Earth Science of the Chinese Academy of Sciences, Beijing, 100101, China

    Shiping Wang

  4. Key Laboratory of Ecosystem Network Observation and Modelling, Institute of Geographic Sciences and Natural Resources Research, the Chinese Academy of Sciences, Beijing, 100101, China

    Xingliang Xu & Yakov Kuzyakov

  5. China–Australia Centre for Sustainable Urban Development, School of Environmental Science and Engineering, Tianjin University, Tianjin, 300072, China

    Lei Zhong

  6. Department of Forest Ecology and Management, Swedish University of Agricultural Sciences, 901 83, Umeå, Sweden

    Paul Kardol

  7. National Hulunber Grassland Ecosystem Observation and Research Station / Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Beijing, 100081, China

    Qiang Yu

  8. Department of Scientific Research Administration, Hulunbuir College, Inner Mongolia, 021008, China

    Changshun Wang

  9. Center for Watershed Ecology, Institute of Life Sciences, Nanchang University, Nanchang, 330031, China

    Zhichun Lan

  10. College of Life Sciences, University of the Chinese Academy of Sciences, Beijing, 100049, China

    Pang Zhe & Yanfen Wang

  11. Department of Soil Science of Temperate Ecosystems, Department of Agricultural Soil Science, University of Göttingen, Göttingen, Germany

    Yakov Kuzyakov

  12. School of Environment, Natural Resources and Geography, Bangor University, Gwynedd, LL57 2UW, UK

    Davey L. Jones

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  1. Lili Jiang
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  2. Shiping Wang
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  3. Pang Zhe
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  4. Changshun Wang
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  6. Lei Zhong
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  7. Qiang Yu
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  9. Yanfen Wang
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  10. Xingliang Xu
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  11. Yakov Kuzyakov
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  12. Caiyun Luo
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  13. Zhenhua Zhang
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  14. Davey L. Jones
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Correspondence to Lili Jiang.

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Jiang, L., Wang, S., Zhe, P. et al. Effects of grazing on the acquisition of nitrogen by plants and microorganisms in an alpine grassland on the Tibetan plateau. Plant Soil 416, 297–308 (2017). https://doi.org/10.1007/s11104-017-3205-1

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