Skip to main content

Advertisement

Log in

Responses of root exudation and nutrient cycling to grazing intensities and recovery practices in an alpine meadow: An implication for pasture management

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Background and aims

The rhizosphere priming effect is caused by root carbon (C) exudation into the rhizosphere; the role of this effect in nutrient cycling and ecosystem recovery of natural grasslands as affected by different grazing intensities is still unknown. The objective of the present study was to investigate the relationships among root C exudation, rhizospheric microbial activity, and their influences on plant nutrient uptake during grazing and recovery periods.

Methods

Field experiments were conducted in the Hongyuan Alpine Meadow to measure root exudation rate and nutrient cycling processes of the dominant species Elymus nutans. Three grazing intensities (an ungrazed control, moderate grazing and heavy grazing) were introduced for two months, following which all treatments received a recovery practice (no grazing for 21 days).

Results

Heavy grazing significantly decreased root exudation rate, soil nitrogen (N) mineralization rate, β-1,4-glucosidase (BG) activity, and foliar C concentration, while moderate grazing had no influence on these parameters compared to the control. After the 21 days of recovery, all these parameters, except N mineralization rate and foliar C concentrations in the heavy grazing treatment, returned to similar levels as in the control, whereas root exudation rate and BG activity rose to even higher levels. Meanwhile, moderate grazing significantly promoted root exudation rate, soil inorganic N concentration, net soil N mineralization rate, and β-N-acetylglucosaminidase (NAG) activity during the recovery stage as compared to the control. Foliar quality was also improved by the recovery practice, indicating that the high availability of N and P is a consequence of the positive root–microbe feedback and will ultimately benefit grazers.

Conclusions

The flush of labile C released to the rhizosphere by grazed plants stimulated extracellular enzyme activities, enhanced soil N mineralization, and increased plant nutrient uptake. These results imply that reasonable (i.e. moderate) grazing followed by a recovery practice can effectively restore and strengthen grassland vegetation, and contribute to the sustainable use of alpine meadows such as Hongyuan.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Arevalo JR, de Nascimento L, Fernandez-Lugo S, Mata J, Bermejo L (2011) Grazing effects on species composition in different vegetation types (La Palma, Canary Island). Acta Oecol 37:230–238

    Article  Google Scholar 

  • Ayres E, Dromph KM, Cook R, Ostle N, Bardgett RD (2007) The influence of below-ground herbivory and defoliation of a legume on nitrogen transfer to neighbouring plants. Funct Ecol 21:256–263

    Article  Google Scholar 

  • Bai WM, Fang Y, Zhou M, Xie T, Li LH, Zhang WH (2015) Heavily intensified grazing reduces root production in an Inner Mongolia temperate steppe. Agric Ecosyst Environ 200:143–150

    Article  Google Scholar 

  • Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266

    Article  CAS  PubMed  Google Scholar 

  • Banks T (2003) Property rights reform in rangeland China: dilemmas on the road to the household ranch. World Dev 31:2129–2142

    Article  Google Scholar 

  • Bardgett RD, van der Putten WH (2014) Belowground biodiversity and ecosystem functioning. Nature 515:505–511

    Article  CAS  PubMed  Google Scholar 

  • Bardgett RD, Wardle DA (2003) Herbivore-mediated linkages between aboveground and belowground communities. Ecology 84:2258–2268

    Article  Google Scholar 

  • Bardgett RD, Wardle DA (2010) Aboveground-belowground linkages: biotic interactions, ecosystem processes, and global change. Oxford University Press, New York

    Google Scholar 

  • Beltran-Garcia MJ, White JF, Prado FM, Prieto KR, Yamaguchi LF, Torres MS, Kato MJ, Medeiros MHG, Mascio PD (2014) Nitrogen acquisition in Agave tequilana from degradation of endophytic bacteria. Scientific Reports 4:6938

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blume-Werry G, Wilson SD, Kreyling J, Milbau A (2016) The hidden season: growing season is 50% longer below than above ground along an arctic elevation gradient. New Phytol 209:978–986

    Article  CAS  PubMed  Google Scholar 

  • Cao JJ, Holden NM, LÜ X, Du GZ (2011) The effect of grazing management on plant species richness on the Qinghai-Tibetan plateau. Grass Forage Sci 66:333–336

    Article  Google Scholar 

  • De Deyn GB, Cornelissen JHC, Bardgett RD (2008) Plant functional traits and soil carbon sequestration in contrasting biomes. Ecol Lett 11:516–531

    Article  PubMed  Google Scholar 

  • Ferrieri AP, Agtuca B, Appel HM, Ferrieri RA, Schultz JC (2013) Temporal changes in allocation and partitioning of new carbon as 11C elicited by simulated herbivory suggest that root shape aboveground responses in Arabidopsis. Plant Physiol 161:692–704

    Article  CAS  PubMed  Google Scholar 

  • Fontaine S, Henault C, Aamor A, Bdioui N, Bloor JMG, Maire V, Mary B, Revaillot S, Maron PA (2011) Fungi mediate long term sequestration of carbon and nitrogen in soil through their priming effect. Soil Biol Biochem 43:86–96

    Article  CAS  Google Scholar 

  • Fontaine S, Mariotti A, Abbadie L (2003) The priming effect of organic matter: a question of microbial competition? Soil Biol Biochem 35:837–843

    Article  CAS  Google Scholar 

  • Frank DA, Groffman PM (2009) Plant rhizospheric N processes: what we don't know and why we should care. Ecology 90:1512–1519

    Article  PubMed  Google Scholar 

  • Hamilton EW, Frank DA (2001) Can plants stimulate soil microbes and their own nutrient supply? Evidence from a grazing tolerant grass. Ecology 82:239–244

    Article  Google Scholar 

  • Hamilton EW, Frank DA, Hinchey PM, Murray TR (2008) Defoliation induces root exudation and triggers positive rhizospheric feedbacks in a temperate grassland. Soil Biol Biochem 40:2865–2873

    Article  CAS  Google Scholar 

  • He NP, Zhang YH, Yu Q, Chen QS, Pan QM, Zhang GM, Han XG (2011) Grazing intensity impacts soil carbon and nitrogen storage of continental steppe. Ecosphere 2:1–10

    Article  Google Scholar 

  • Henry F, Vestergard M, Christensen S (2008) Evidence for a transient increase of rhizodeposition within one and a half day after a severe defoliation of Plantago arenaria grown in soil. Soil Biol Biochem 40:1264–1267

    Article  CAS  Google Scholar 

  • Hiernaux P (1998) Effects of grazing on plant species composition and spatial distribution in rangelands of the Sahel. Plant Ecol 138:191–202

    Article  Google Scholar 

  • Jackson ML (1964) Soil chemical analysis. Prentice Hall, Englewood Cliffs

    Google Scholar 

  • Kemp DR, Han GD, Hou XY, Michalk DL, Hou FJ, Wu JP, Zhang YJ. 2013. Innovative grassland management systems for environmental and livelihood benefits. Proceedings of National Academy of Sciences USA, 110: 8369-8374

  • Klumpp K, Fontaine S, Attard E, LeRoux X, Gleixner G, Soussana JF (2009) Grazing triggers soil carbon loss by altering plant roots and their control on soil microbial community. J Ecol 97:876–885

    Article  CAS  Google Scholar 

  • Li WJ, Ali S, Zhang Q (2007) Property rights and grassland degradation: a study of the Xilingol pasture, Inner Mongolia, China. J Environ Manag 85:461–470

    Article  Google Scholar 

  • Medina-Roldan E, Paz-Ferreiro J, Bardgett RD (2012) Grazing exclusion affects soil and plant communities, but has no impact on soil carbon storage in an upland grassland. Agric Ecosyst Environ 149:118–123

    Article  Google Scholar 

  • Meier IC, Pritchard SG, Brzostek ER, McCormack ML, Phillips RP (2015) The rhizosphere and hyphosphere differ in their impacts on carbon and nitrogen cycling in forests exposed to elevated CO2. New Phytol 205:1164–1174

    Article  CAS  PubMed  Google Scholar 

  • Olsen YS, Dausse A, Garbutt A, Ford H, Thomas DN, Jones DL (2011) Cattle grazing drives nitrogen and carbon cycling in a temperate salt marsh. Soil Biol Biochem 43:531–541

    Article  CAS  Google Scholar 

  • Phillips RP, Erlitz Y, Bier R, Bernhardt ES (2008) A new approach for capturing soluble root exudates in forest soils. Funct Ecol 22:990–999

    Article  Google Scholar 

  • Phillips RP, Finzi AC, Bernhardt ES (2011) Enhanced root exudation induces microbial feedbacks to N cycling in a pine forest under long-term CO2 fumigation. Ecol Lett 14:187–194

    Article  PubMed  Google Scholar 

  • Phillips RP, Midgley MG, Brozstek E (2013) The mycorrhizal-associated nutrient economy: a new framework for predicting carbon-nutrient couplings in forests. New Phytol 199:41–51

    Article  CAS  PubMed  Google Scholar 

  • Schimel J, Balser TC, Wallenstein M (2007) Microbial stress-response physiology and its implications for ecosystem function. Ecology 88:1386–1394

    Article  PubMed  Google Scholar 

  • Seagle SW, McNaughton SJ, Ruess RW (1992) Simulated effects of grazing on soil nitrogen and mineralisation in contrasting Serengeti grasslands. Ecology 73:1105–1123

    Article  Google Scholar 

  • Shahzad T, Chenu C, Repincay C, Mougin C, Ollier JL, Fontaine S (2012) Plant clipping decelerates the mineralization of recalcitrant soil organic matter under multiple grassland species. Soil Biol Biochem 51:73–80

    Article  CAS  Google Scholar 

  • Shi CG, Silva LCR, Zhang HX, Zheng QY, Xiao BX, Wu N, Sun G (2015) Climate warming alters nitrogen dynamics and total non-structural carbohydrate accumulations of perennial herbs of distinctive functional groups during the plant senescence in autumn in an alpine meadow of the Tibetan plateau, China. Agric For Meteorol 200:21–29

    Article  Google Scholar 

  • Smith WH (1976) Character and significance of forest tree root exudates. Ecology 57:324–331

    Article  CAS  Google Scholar 

  • Strickland MS, Rousk J (2010) Considering fungal: bacterial dominance in soil – methods, controls, and ecosystem implications. Soil Biol Biochem 42:1385–1395

    Article  CAS  Google Scholar 

  • Sun J, Wang X, Cheng G, Wu J, Hong J, Niu S (2014) Effect of grazing regimes on plant traits and soil nutrients in an alpine steppe, northern Tibetan plateau. PLoS One 9:e108821

    Article  PubMed  PubMed Central  Google Scholar 

  • van der Heijden MGA, Bardgett RD, van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310

    Article  PubMed  Google Scholar 

  • Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass. Soil Biol Biochem 19:703–707

    Article  CAS  Google Scholar 

  • Wang R, Dorodnikow M, Yang S, Zhang Y, Filley TR, Turco RF, Zhang Y, Xu Z, Li H, Jiang Y (2015) Responses of enzymatic activities within soil aggregates to 9-year nitrogen and water addition in a semi-arid grassland. Soil Biol Biochem 81:159–167

    Article  CAS  Google Scholar 

  • Xu MY, Xie F, Wang K (2014) Responses of vegetation and soil carbon and nitrogen storage to grazing intensity in semi-arid grasslands in the agro-pastoral zone of northern China. PLoS One 9:e96604

    Article  PubMed  PubMed Central  Google Scholar 

  • Yin HJ, Wheeler E, Phillips RP (2014) Root-induced changes in nutrient cycling in forests depend on exudation rates. Soil Biol Biochem 78:213–221

    Article  CAS  Google Scholar 

  • Zhang YJ, Huang D, Badgery WB, Kemp DR, Chen WQ, Wang XY, Liu N (2015) Reduced grazing pressure delivers production and environmental benefits for the typical steppe of north China. Scientific Reports 5:16434

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank Timothy A. Doane, anonymous reviewers and Accdon/Let Pub Experts for their thoughtful comments, which helped in improving the manuscript. This work was supported by the National Science Foundation of China (Nos. 31350110328, 31500346 and 41361076), the Ministry of Science and Technology of the People’s Republic of China (2016YFC0501803), the Chinese Academy of Sciences (KFJ-SW-STS-177, Western Light Program), the Sichuan Science & Technology Bureau (2015HH0025, 2015JY0231, 2016HH0082 and 2016JY0117) and the Youth Professor Program of Chengdu Institute of Biology.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Geng Sun or Yanbao Lei.

Additional information

Responsible Editor: Tim S. George.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sun, G., Zhu-Barker, X., Chen, D. et al. Responses of root exudation and nutrient cycling to grazing intensities and recovery practices in an alpine meadow: An implication for pasture management. Plant Soil 416, 515–525 (2017). https://doi.org/10.1007/s11104-017-3236-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-017-3236-7

Keywords

Navigation