Skip to main content
Log in

Keystone Perennial Grassland Species Control Soil Nitrogen Flows

  • Published:
Ecosystems Aims and scope Submit manuscript

Abstract

Restoration of many grassland ecosystems is dependent on restoring native N cycling regimes, through methods such as nutrient stripping, C addition, and/or re-establishment of keystone species. We studied topsoil N pools and fluxes under five different understorey vegetation communities of different degradation states of grassy eucalypt woodlands across 11 sites in New South Wales, Australia, in order to identify whether high N flux but low standing N concentrations were responsible for the success of reference Themeda triandra communities. The presence of NO3 was the main differentiator between the annual exotic (AE) and reference states, which both demonstrated twofold-threefold increases N flux relative to the depleted states. Reference states were characterised by high proteolysis and dissolved organic N (DON) mineralisation rates, but also low δ15N and a high C:N ratio, which taken together indicate fresh organic matter inputs that turn over quickly. In quantifying fast rates of N cycling yet low NO3 pools in the reference states, our data highlight a productive ecosystem dominated by rapidly cycling DON rather than NO3 in its reference state. The higher NO3 concentrations coupled with fast N cycling in the degraded AE state indicate that although available N production is high in both systems, uptake is lower in the AE state, perpetuating a larger standing NO3 pool that may prevent re-establishment of native species. Steps that promote rapid DON cycling while inhibiting nitrification may lead to a soil biogeochemical status more suitable for the restoration of highly productive native grasslands.

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.

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6

Similar content being viewed by others

References

  • Allan E, Manning P, Alt F, Binkenstein J, Blaser S, Bluethgen N, Boehm S, Grassein F, Hoelzel N, Klaus VH, Kleinebecker T, Morris EK, Oelmann Y, Prati D, Renner SC, Rillig MC, Schaefer M, Schloter M, Schmitt B, Schoening I, Schrumpf M, Solly E, Sorkau E, Steckel J, Steffen-Dewenter I, Stempfhuber B, Tschapka M, Weiner CN, Weisser WW, Werner M, Westphal C, Wilcke W, Fischer M. 2015. Land use intensification alters ecosystem multifunctionality via loss of biodiversity and changes to functional composition. Ecology Letters 18:834–43.

    Article  PubMed  PubMed Central  Google Scholar 

  • Anderson MJ, Willis TJ. 2003. Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84:511–25.

    Article  Google Scholar 

  • Bray JR, Gorham E. 1964. Litter Production in Forests of the World. Advances in Ecological Research 2:101–57.

    Article  Google Scholar 

  • Bueno A, Pritsch K, Simon J. 2019. Species-specific outcome in the competition for nitrogen between invasive and native tree seedlings. Frontiers in Plant Science 10:29.

    Article  Google Scholar 

  • Craine JM, Brookshire ENJ, Cramer MD, Hasselquist NJ, Koba K, Marin-Spiotta E, Wang L. 2015. Ecological interpretations of nitrogen isotope ratios of terrestrial plants and soils. Plant and Soil:1–26.

  • Creamer CA, Filley TR, Olk DC, Stott DE, Dooling V, Boutton TW. 2013. Changes to soil organic N dynamics with leguminous woody plant encroachment into grasslands. Biogeochemistry 113:307–21.

    Article  CAS  Google Scholar 

  • de Vries FT, Bardgett RD. 2016. Plant community controls on short-term ecosystem nitrogen retention. New Phytologist 210:861–74.

    Article  Google Scholar 

  • Fanin N, Gundale MJ, Farrell M, Ciobanu M, Baldock JA, Nilsson M-C, Kardol P, Wardle DA. 2018. Consistent effects of biodiversity loss on multifunctionality across contrasting ecosystems. Nature Ecology & Evolution 2:269–78.

    Article  Google Scholar 

  • Farrell M, Healey JR, Godbold DL, Nason MA, Tandy S, Jones DL. 2011a. Modification of fertility of soil materials for restoration of acid grassland habitat. Restoration Ecology 19:509–19.

    Article  Google Scholar 

  • Farrell M, Hill PW, Farrar J, Bardgett RD, Jones DL. 2011b. Seasonal variation in soluble soil carbon and nitrogen across a grassland productivity gradient. Soil Biology and Biochemistry 43:835–44.

    Article  CAS  Google Scholar 

  • Farrell M, Hill PW, Wanniarachchi SD, Farrar J, Bardgett RD, Jones DL. 2011c. Rapid peptide metabolism: a major component of soil nitrogen cycling? Global Biogeochemical Cycles 25:3014.

    Article  CAS  Google Scholar 

  • Fischer J, Stott J, Zerger A, Warren G, Sherren K, Forrester RI. 2009. Reversing a tree regeneration crisis in an endangered ecoregion. Proceedings of the National Academy of Sciences of the United States of America 106:10386–91.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harpole WS, Sullivan LL, Lind EM, Firn J, Adler PB, Borer ET, Chase J, Fay PA, Hautier Y, Hillebrand H, MacDougall AS, Seabloom EW, Williams R, Bakker JD, Cadotte MW, Chaneton EJ, Chu C, Cleland EE, D’Antonio C, Davies KF, Gruner DS, Hagenah N, Kirkman K, Knops JMH, La Pierre KJ, McCulley RL, Moore JL, Morgan JW, Prober SM, Risch AC, Schuetz M, Stevens CJ, Wragg PD. 2016. Addition of multiple limiting resources reduces grassland diversity. Nature 537:93–6.

    Article  CAS  PubMed  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. Nature Climate Change 1:50–3.

    Article  CAS  Google Scholar 

  • Hodge A, Storer K. 2015. Arbuscular mycorrhiza and nitrogen: implications for individual plants through to ecosystems. Plant and Soil 386:1–19.

    Article  CAS  Google Scholar 

  • Hofmockel KS, Fierer N, Colman BP, Jackson RB. 2010. Amino acid abundance and proteolytic potential in North American soils. Oecologia 163:1069–78.

    Article  PubMed  Google Scholar 

  • Jiang L, Wang S, Zhe P, Xu X, Kardol P, Li Y, Zhang L, Wang Y, Lei Z, Lan Z, Hill PW, Zhang Z, Luo C, Rui Y, Ning D, Jones DL. 2018. Plant organic N uptake maintains species dominance under long-term warming. Plant and Soil 433:243–55.

    Article  CAS  Google Scholar 

  • Jones DL, Owen AG, Farrar J. 2002. Simple method to enable the high resolution determination of total free amino acids in soil solutions and soil extracts. Soil Biology and Biochemistry 34:1893–902.

    Article  CAS  Google Scholar 

  • Kardol P, Van der Wal A, Bezemer TM, de Boer W, Duyts H, Holtkamp R, Van der Putten WH. 2008. Restoration of species-rich grasslands on ex-arable land: Seed addition outweighs soil fertility reduction. Biological Conservation 141:2208–17.

    Article  Google Scholar 

  • Kaur B, Kaur G, Asthir B. 2017. Biochemical aspects of nitrogen use efficiency: An overview. Journal of Plant Nutrition 40:506–23.

    Article  CAS  Google Scholar 

  • Ludwig JA. 2011. Restoring disturbed landscapes: Putting principles into practice. Washington: Island Press.

    Google Scholar 

  • Marin-Spiotta E, Silver WL, Swanston CW, Ostertag R. 2009. Soil organic matter dynamics during 80 years of reforestation of tropical pastures. Global Change Biology 15:1584–97.

    Article  Google Scholar 

  • McArdle BH, Anderson MJ. 2001. Fitting multivariate models to community data: A comment on distance-based redundancy analysis. Ecology 82:290–7.

    Article  Google Scholar 

  • Miranda KM, Espey MG, Wink DA. 2001. A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide-Biology and Chemistry 5:62–71.

    Article  CAS  PubMed  Google Scholar 

  • Mulvaney RL. 1996. Nitrogen—inorganic forms. In: Sparks DL, Page AL, Helmke PA, Loeppert RH, Soltanpour PN, Tabatabai MA, Johnston CT, Sumner ME, Bartels JM, Bigham JM, editors. methods of soil analysis part-3. Vol. sssabookseries. SSSA Book Series. Madison, WI: Soil Science Society of America, American Society of Agronomy. pp 1123–84.

  • Murphy DV, Macdonald AJ, Stockdale EA, Goulding KWT, Fortune S, Gaunt JL, Poulton PR, Wakefield JA, Webster CP, Wilmer WS. 2000. Soluble organic nitrogen in agricultural soils. Biology and Fertility of Soils 30:374–87.

    Article  CAS  Google Scholar 

  • Murphy DV, Recous S, Stockdale EA, Fillery I, Jensen LS, Hatch DJ, Goulding K. 2003. Gross nitrogen fluxes in soil: Theory, measurement and application of N-15 pool dilution techniques. Advances in Agronomy 79:69–118.

    Article  CAS  Google Scholar 

  • Natelhoffer KJ, Fry B. 1988. Controls on natural nitrogen-15 and carbon-13 abundances in forest soil organic matter. Soil Science Society of America Journal 52:1633–40.

    Article  CAS  Google Scholar 

  • Paul EA, Clark FE. 1996. Soil microbiology and biochemistry. Cambridge: Academic Press.

    Google Scholar 

  • Perry LG, Blumenthal DM, Monaco TA, Paschke MW, Redente EF. 2010. Immobilizing nitrogen to control plant invasion. Oecologia 163:13–24.

    Article  PubMed  Google Scholar 

  • Power ME, Tilman D, Estes JA, Menge BA, Bond WJ, Mills LS, Daily G, Castilla JC, Lubchenco J, Paine RT. 1996. Challenges in the Quest for Keystones. Bioscience 46:609–620.

    Article  Google Scholar 

  • Prober SM, Lunt ID, Thiele KR. 2002a. Determining reference conditions for management and restoration of temperate grassy woodlands: Relationships among trees, topsoils and understorey flora in little-grazed remnants. Australian Journal of Botany 50:687–97.

    Article  Google Scholar 

  • Prober SM, Stol J, Piper M, Gupta VVSR, Cunningham SA. 2014a. Enhancing soil biophysical condition for climate-resilient restoration in mesic woodlands. Ecological Engineering 71:246–55.

    Article  Google Scholar 

  • Prober SM, Stol J, Piper M, Gupta VVSR, Cunningham SA. 2014b. Towards climate-resilient restoration in mesic eucalypt woodlands: Characterizing topsoil biophysical condition in different degradation states. Plant and Soil 383:231–44.

    Article  CAS  Google Scholar 

  • Prober SM, Thiele KR, Lunt ID, Koen TB. 2005. Restoring ecological function in temperate grassy woodlands: Manipulating soil nutrients, exotic annuals and native perennial grasses through carbon supplements and spring burns. Journal of Applied Ecology 42:1073–85.

    Article  CAS  Google Scholar 

  • Prober SM, Thiele KR, Lunt ID. 2002b. Identifying ecological barriers to restoration in temperate grassy woodlands: Soil changes associated with different degradation states. Australian Journal of Botany 50:699–712.

    Article  CAS  Google Scholar 

  • Rayment GE, Lyons DJ. 2011. Soil chemical methods. CSIRO Publishing.

  • Schimel JP, Bennett J. 2004. Nitrogen mineralization: Challenges of a changing paradigm. Ecology 85:591–602.

    Article  Google Scholar 

  • Seabloom EW, Borer ET, Boucher VL, Burton RS, Cottingham KL, Goldwasser L, Gram WK, Kendall BE, Micheli F. 2003. Competition, seed limitation, disturbance, and reestablishment of California native annual forbs. Ecological Applications 13:575–92.

    Article  Google Scholar 

  • Simpson J, Warren C, Adams P. 2017. Potential protease activity and organic nitrogen concentration are rapid tests and accurate indicators of N-availability in Tasmanian Eucalyptus nitens plantations. Soil Biology and Biochemistry 115:152–60.

    Article  CAS  Google Scholar 

  • Stark JM, Norton JM. 2015. The invasive annual cheatgrass increases nitrogen availability in 24-year-old replicated field plots. Oecologia 177:799–809.

    Article  PubMed  Google Scholar 

  • Steel RGD, Torrie JH. 1981. Principles and procedures of statistics. McGraw-Hill.

  • Tandy S, Wallace HL, Jones DL, Nason MA, Williamson JC, Healey JR. 2011. Can a mesotrophic grassland community be restored on a post-industrial sandy site with compost made from waste materials? Biological Conservation 144:500–10.

    Article  Google Scholar 

  • Voroney RP, Brookes PC, Beyaert RP. 2008. Soil microbial biomass C, N, P, and S. In: Carter MR, Gregorich EG, editors. Soil sampling and methods of analysis. 2nd ed. Boca Raton, FL. pp 637–51.

  • Walker KJ, Stevens PA, Stevens DP, Mountford JO, Manchester SJ, Pywell RF. 2004. The restoration and re-creation of species-rich lowland grassland on land formerly managed for intensive agriculture in the UK. Biological Conservation 119:1–18.

    Article  Google Scholar 

  • Wanek W, Mooshammer M, Bloechl A, Hanreich A, Richter A. 2010. Determination of gross rates of amino acid production and immobilization in decomposing leaf litter by a novel N-15 isotope pool dilution technique. Soil Biology and Biochemistry 42:1293–302.

    Article  CAS  Google Scholar 

  • Warren CR. 2013a. High diversity of small organic N observed in soil water. Soil Biology and Biochemistry 57:444–50.

    Article  CAS  Google Scholar 

  • Warren CR. 2013b. Quaternary ammonium compounds can be abundant in some soils and are taken up as intact molecules by plants. New Phytologist 198:476–85.

    Article  CAS  Google Scholar 

  • Warren CR. 2014. Organic N molecules in the soil solution: What is known, what is unknown and the path forwards. Plant and Soil 375:1–19.

    Article  CAS  Google Scholar 

  • Yang WH, Ryals RA, Cusack DF, Silver WL. 2017. Cross-biome assessment of gross soil nitrogen cycling in California ecosystems. Soil Biology and Biochemistry 107:144–55.

    Article  CAS  Google Scholar 

  • Yu W, Brookes PC, Ma Q, Zhou H, Xu Y, Shen S. 2011. Extraction of soil nitrogen by chloroform fumigation—A new index for the evaluation of soil nitrogen supply. Soil Biology and Biochemistry 43:2423–6.

    Article  CAS  Google Scholar 

  • Zhu F, Dai L, Hobbie EA, Koba K, Liu X, Gurmesa GA, Huang S, Li S, Li Y, Han S, Fang Y. 2019. Uptake Patterns of Glycine, Ammonium, and Nitrate Differ Among Four Common Tree Species of Northeast China. Frontiers in Plant Science 10:1388.

    Article  Google Scholar 

Download references

Acknowledgements

This study was supported by the CSIRO Sustainable Agriculture Flagship and the Australian government through Caring for our Country. We thank Jacqui Stol and Melissa Piper for field assistance, Tom Carter for laboratory assistance, J. Speijers for statistical advice, and the many land managers who allowed us to sample their woodlands.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mark Farrell.

Ethics declarations

Conflict of interest

The authors state that there are no conflict of interest.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 165 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Farrell, M., Prober, S.M. Keystone Perennial Grassland Species Control Soil Nitrogen Flows. Ecosystems 24, 1500–1515 (2021). https://doi.org/10.1007/s10021-020-00597-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10021-020-00597-2

Keywords

Navigation