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Oecologia

, Volume 189, Issue 1, pp 255–266 | Cite as

Clonality-dependent dynamic change of plant community in temperate grasslands under nitrogen enrichment

  • Zhi Zheng
  • Wenming Bai
  • Wen-Hao ZhangEmail author
Global change ecology – original research

Abstract

Clonal plants with diverse growth forms are dominant in plant community of temperate grasslands and sensitive to enhanced atmospheric nitrogen (N) deposition. However, whether and how clonal plants with different growth forms differ in their responses to N deposition remains unclear. We investigated the long-term (14-year) and short-term (4-year) effects of N addition on clonal plants of three growth forms (clumper, stoloniferous and rhizomatous clonal plants) in temperate grasslands of northern China by monitoring the clonal traits and belowground meristems. We found that, for the first time, the effects of N addition on clonal plants were dependent on N-addition duration and growth forms of clonal plants. Short-term N addition enhanced growth of clumper clonal plants, while long-term N addition favored growth of rhizomatous clonal plants and suppressed growth of stoloniferous clonal plants. We further revealed that clumper clonal plants can preempt space by tillering rapidly, thus conferring their dominance in the community and suppressing vegetative reproduction of stoloniferous clonal plants upon exposure to short-term N enhancement. In contrast, long-term N addition depressed initiation of buds and tillering of clumper clonal plants. Moreover, long-term N addition shortened rhizome internode and enhanced vegetative reproduction of rhizomatous clonal plants, leading to their ultimate dominance in the steppe community. Our results highlight the important roles of belowground meristems and clonal traits in control of dynamic changes of plant community in response to N enrichment. These findings provide a new perspective to understand N-induced changes in plant community of temperate grasslands.

Keywords

Nitrogen deposition Clonal plants Growth form Nitrogen-addition duration Temperate steppe 

Notes

Acknowledgments

We appreciate the constructive suggestions made by the editors and anonymous reviewers on previous version of the manuscript. We thank Professor Gary G. Mittelbach from Michigan State University and Timothy L. Dickson from University of Nebraska Omaha for thoughtful comments on earlier version of the manuscript. We also thank all the field assistance that contributed to this study and staff at the Doulun Restoration Ecology Research Station, Institute of Botany, Chinese Academy of sciences for their help in maintaining the field facilities. The work was supported by National Natural Science Foundation of China (31830011, 31570403 and 31470466).

Author contribution statement

WZ and ZZ conceived the ideas and designed methodology; ZZ and WB carried out field work; ZZ and WZ analyzed the data; ZZ and WZ wrote the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

442_2018_4317_MOESM1_ESM.docx (3.1 mb)
Supplementary material 1 (DOCX 3192 kb)

References

  1. Adachi N, Terashima I, Takahashi M (1996) Central dieback of monoclonal stands of Reynoutria japonica in an early stage of primary succession on Mount Fuji. Ann Bot 77:477–486.  https://doi.org/10.1006/anbo.1996.0058 CrossRefGoogle Scholar
  2. Bai Y, Han X, Wu J, Chen Z, Li L (2004) Ecosystem stability and compensatory effects in the inner mongolia grassland. Nature 431:181–184.  https://doi.org/10.1038/nature02850 CrossRefPubMedGoogle Scholar
  3. Bai Y, Wu J, Clark CM, Naeem S, Pan Q, Huang J, Zhang L, Han X (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.  https://doi.org/10.1111/j.1365-2486.2009.02142.x CrossRefGoogle Scholar
  4. Benson EJ, Hartnett DC (2006) The role of seed and vegetative reproduction in plant recruitment and demography in tallgrass prairie. Plant Ecol 187:163–178.  https://doi.org/10.1007/s11258-005-0975-y CrossRefGoogle Scholar
  5. Bobbink R, Hicks K, Galloway J, Spranger T, Alkemade R, Ashmore M, Bustamante M, Cinderby S, Davidson E, Dentener F, Emmett B, Erisman JW, Fenn M, Gilliam F, Nordin A, Pardo L, De Vries W (2010) Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis. Ecol Appl 20:30–59.  https://doi.org/10.1890/08-1140.1 CrossRefPubMedGoogle Scholar
  6. Bonanomi G, Incerti G, Stinca A, Cartenì F, Giannino F, Mazzoleni S (2014) Ring formation in clonal plants. Commun Ecol 15:77–86.  https://doi.org/10.1556/ComEc.15.2014.1.8 CrossRefGoogle Scholar
  7. Bowman WD, Cleveland CC, Ĺuboš Halada, Hreško J, Baron JS (2008) Negative impact of nitrogen deposition on soil buffering capacity. Nat Geosci 1:767–770.  https://doi.org/10.1038/ngeo339 CrossRefGoogle Scholar
  8. Briske DD, Derner JD (1998) Clonal biology of caespitose grasses. In: Cheplick G (ed) Population ecology of grasses. Cambridge University Press, Cambridge, pp 106–135CrossRefGoogle Scholar
  9. Clark CM, Tilman D (2008) Loss of plant species after chronic low-level nitrogen deposition to prairie grasslands. Nature 451:712–715.  https://doi.org/10.1038/nature06503 CrossRefPubMedGoogle Scholar
  10. Dalgleish HJ, Hartnett DC (2006) Below-ground bud banks increase along a precipitation gradient of the North American Great Plains: a test of the meristem limitation hypothesis. New Phytol 171:81–89.  https://doi.org/10.1111/j.1469-8137.2006.01739.x CrossRefPubMedGoogle Scholar
  11. de Kroon H, Huber H, Stuefer JF, Groenendael JMV (2005) A modular concept of phenotypic plasticity in plants. New Phytol 166:73–82.  https://doi.org/10.1111/j.1469-8137.2004.01310.x CrossRefPubMedGoogle Scholar
  12. DeMalach N, Zaady E, Kadmon R (2017) Light asymmetry explains the effect of nutrient enrichment on grassland diversity. Ecol Lett 20:60–69.  https://doi.org/10.1111/ele.12706 CrossRefPubMedGoogle Scholar
  13. Dickson DL, Gross KL (2013) Plant community responses to long-term fertilization: changes in functional group abundance drive changes in species richness. Oecologia 173:1513–1520.  https://doi.org/10.1007/s00442-013-2722-8 CrossRefPubMedGoogle Scholar
  14. Dickson TL, Mittelbach GG, Reynolds HL, Gross KL (2016) Height and clonality traits determine plant community responses to fertilization. Ecology 95:2443–2452.  https://doi.org/10.1890/13-1875.1 CrossRefGoogle Scholar
  15. Eilts JA, Mittelbach GG, Reynolds HL, Gross KL (2011) Resource heterogeneity, soil fertility, and species diversity: effects of clonal species on plant communities. Am Nat 177:574–588.  https://doi.org/10.1086/659633 CrossRefPubMedGoogle Scholar
  16. Eriksson O (1986) Mobility and space capture in the stoloniferous plant Potentilla anserine. Oikos 46:82–87.  https://doi.org/10.2307/3565383 CrossRefGoogle Scholar
  17. Fischer M, Kleunen MV (2001) On the evolution of clonal plant life histories. Evol Ecol 15:565–582.  https://doi.org/10.1023/A:1016013721469 CrossRefGoogle Scholar
  18. Foster B, Gross KL (1998) Species richness in a successional grassland: effects of nitrogen enrichment and litter. Ecology 79:2593–2602.  https://doi.org/10.2307/176503 CrossRefGoogle Scholar
  19. Gough L, Goldberg DE, Hershock C, Pauliukonis N, Petru M (2002) Investigating the community consequences of competition among clonal plants. In: Stuefer JF, Erschbamer B, Huber HH, Suzuki JI (eds) Ecology and evolutionary biology of clonal plants. Springer, Dordrecht.  https://doi.org/10.1007/978-94-017-1345-0_18 CrossRefGoogle Scholar
  20. Gough L, Gross KL, Cleland EE, Clark CM, Collins SL, Fargione JE, Pennings SC, Suding KN (2012) Incorporating clonal growth form clarifies the role of plant height in response to nitrogen addition. Oecologia 169:1053–1062.  https://doi.org/10.1007/s00442-012-2264-5 CrossRefPubMedGoogle Scholar
  21. Greaver TL, Clark CM, Compton JE, Vallano D, Talhelm AF, Weaver CP et al (2016) Key ecological responses to nitrogen are altered by climate change. Nat Clim Change 6:836–843.  https://doi.org/10.1038/nclimate3088 CrossRefGoogle Scholar
  22. Grime JM (1973) Competitive exclusion in herbaceous vegetation. Nature 242:344–347.  https://doi.org/10.1038/242344a0 CrossRefGoogle Scholar
  23. Gross KL, Mittelbach GG (2017) Negative effects of fertilization on grassland species richness are stronger when tall clonal species are present. Folia Geobot 52:401–409.  https://doi.org/10.1007/s12224-017-9300-5 CrossRefGoogle Scholar
  24. 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 JM, 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 537:93–96.  https://doi.org/10.1038/nature19324 CrossRefPubMedGoogle Scholar
  25. Hautier Y, Niklaus PA, Hector A (2009) Competition for light causes plant biodiversity loss after eutrophication. Science 324:636–663.  https://doi.org/10.1126/science.1169640 CrossRefPubMedGoogle Scholar
  26. Henry M, Stevens H, Bunker DE, Schnitzer SA et al (2004) Establishment limitation reduces species recruitment and species richness as soil resources rise. J Ecol 92:339–347.  https://doi.org/10.1111/j.0022-0477.2004.00866.x CrossRefGoogle Scholar
  27. Herben T, Nováková Z, Klimešová J (2014) Clonal growth and plant species abundance. Ann Bot 114:377–388.  https://doi.org/10.1093/aob/mct308 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Humphrey LD, Pyke DA (1998) Demographic and growth responses of a guerrilla and a phalanx perennial grass in competitive mixtures. J Ecol 86:854–864.  https://doi.org/10.1046/j.1365-2745.1998.8650854.x CrossRefGoogle Scholar
  29. Isbell F, Reich PB, Tilman D, Hobbie SE, Polasky S, Binder S (2013) Nutrient enrichment, biodiversity loss, and consequent declines in ecosystem productivity. Proc Natl Acad Sci USA 110:11911–11916.  https://doi.org/10.1073/pnas.1310880110 CrossRefPubMedGoogle Scholar
  30. Isbell F, Cowles J, Dee LE, Loreau M, Reich PB (2018) Quantifying effect of biodiversity on ecosystem functioning across times and places. Ecol Lett 21:763–778.  https://doi.org/10.1111/ele.12928 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Kang L, Han X, Zhang Z, Sun OJ (2007) Grassland ecosystems in China: review of current knowledge and research advancement. Philos Trans R Soc Lond B Biol Sci 362:997–1008.  https://doi.org/10.1098/rstb.2007.2029 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Klimešová J, Tackenberg O, Herben T (2016) Herbs are different: clonal and bud bank traits can matter more than leaf-height-seed traits. New Phytol 210:13–17.  https://doi.org/10.1111/nph.13788 CrossRefPubMedGoogle Scholar
  33. Klimešová J, Danihelka J, Chrtek J, Bello F, Herben T (2017) CLO-PLA: a database of clonal and bud-bank traits of the Central European flora. Ecology 98:1179.  https://doi.org/10.1002/ecy.1745 CrossRefPubMedGoogle Scholar
  34. Klimešová J, Martínková J, Herben T (2018) Horizontal growth: an overlooked dimension in plant trait space. Perspect Plant Ecol 32:18–21.  https://doi.org/10.1016/j.ppees.2018.02.002 CrossRefGoogle Scholar
  35. Knapp AK, Smith MD (2001) Variation among biomes in temporal dynamics of aboveground primary production. Science 291:481–484.  https://doi.org/10.1126/science.291.5503.481 CrossRefPubMedGoogle Scholar
  36. Li J, Li Z, Ren J (2005) Effect of grazing intensity on clonal morphological plasticity and biomass allocation patterns of Artemisia frigida and Potentilla acaulis in the Inner Mongolia steppe. N Z J Agric Res 48:57–61.  https://doi.org/10.1080/00288233.2005.9513631 CrossRefGoogle Scholar
  37. Liu X, Zhang Y, Han W, Tang A, Shen J, Cui Z, Vitousek P, Erisman JW, Goulding K, Christie P, Fangmeier A, Zhang F (2013) Enhanced nitrogen deposition over China. Nature 494:459–462.  https://doi.org/10.1038/nature11917 CrossRefPubMedGoogle Scholar
  38. Liu XY, Liang TG, Guo ZG, Long RJ (2014) A rangeland management pattern based on functional classification in the northern Tibetan region of China. Land Degrad Dev 25:193–201.  https://doi.org/10.1002/ldr.2139 CrossRefGoogle Scholar
  39. Liu X, Xu W, Du E, Pan Y, Goulding K (2016) Reduced nitrogen dominated nitrogen deposition in the United States, but its contribution to nitrogen deposition in China decreased. Proc Natl Acad Sci USA 113:E3590.  https://doi.org/10.1073/pnas.1607507113 CrossRefPubMedGoogle Scholar
  40. Lovett Doust L (1981) Population dynamics and local specialisation in a clonal Ranunculus repens. II. The dynamics of ramets in contrasting habitats. J Ecol 69:743–755.  https://doi.org/10.2307/2259634 CrossRefGoogle Scholar
  41. Mittelbach GG (2012) Community ecology. Sinauer Associates Inc, SunderlandGoogle Scholar
  42. Oksanen J (2018) Vegan: community ecology package. R package version 2.5-3. https://CRAN.R-project.org/package=vegan. Accessed 21 Oct 2018
  43. Ott JP, Hartnett DC (2015) Bud bank dynamics and clonal growth strategy in the rhizomayous grass, Pascopyrum smithii. Plant Ecol 216:395–405.  https://doi.org/10.1007/s11258-014-0444-6 CrossRefGoogle Scholar
  44. Ottaviani G, Martínková J, Herben T, Pausas JG, Klimešová J (2017) On plant modularity traits: functions and challenges. Trends Plant Sci 22:648–651.  https://doi.org/10.1016/j.tplants.2017.05.010 CrossRefPubMedGoogle Scholar
  45. Pielou EC (1977) Mathematical ecology. Wiley, New YorkGoogle Scholar
  46. R Development Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.r-project.org/. Accessed Jan 2018
  47. Schmid B (1985) Clonal growth in grassland perennials II. Growth form and fine-scale colonizing ability. J Ecol 73:809–818.  https://doi.org/10.2307/2260148 CrossRefGoogle Scholar
  48. Shannon C, Weaver W (1949) The mathematical theory of communication. University of Illinois Press, ChicagoGoogle Scholar
  49. Sheffer E, Yizhaq H, Gilad E, Shachak M, Meron E (2007) Why do plants in resource-deprived environments form rings? Ecol Complex 4:192–200.  https://doi.org/10.1016/j.ecocom.2007.06.008 CrossRefGoogle Scholar
  50. Simkin SM, Allen EB, Bowman WD, Clark CM, Belnap J, Brooks ML, Cade BS, Collins SL, Geiser LH, Gilliam FS, Jovan SE, Pardo LH, Schulz BK, Stevens CJ, Suding KN, Throop HL, Waller DM (2016) Conditional vulnerability of plant diversity to atmospheric nitrogen deposition across the United States. Proc Natl Acad Sci USA 113:4086–4091.  https://doi.org/10.1073/pnas.1515241113 CrossRefPubMedGoogle Scholar
  51. Stevens CJ, Dise NB, Mountford JO, Gowing DL (2004) Impact of nitrogen deposition on the species richness of grasslands. Science 303:1876–1879.  https://doi.org/10.1126/science.1094678 CrossRefPubMedGoogle Scholar
  52. Strickland R (1987) Hollow crowns: overgrazing, undergrazing, or old age? Rangelands 5:13–14Google Scholar
  53. Suding KN, Collins SL, Gough L, Clark C, Cleland EE, Gross KL, Milchunas DG, Pennings S (2005) Functional-and abundance-based mechanisms explain diversity loss due to N fertilization. Proc Natl Acad Sci USA 102:4387–4392.  https://doi.org/10.1073/pnas.0408648102 CrossRefPubMedGoogle Scholar
  54. Sutherland WJ (1987) Growth and foraging behaviour. Nature 330:18–19.  https://doi.org/10.1038/330018a0 CrossRefGoogle Scholar
  55. Tian QY, Liu NN, Bai WM, Li LH, Zhang WH (2015) Disruption of metal ion homeostasis in soils is associated with nitrogen deposition-induced species loss in an Inner Mongolia steppe. Biogeosciences 12:3499–3512.  https://doi.org/10.5194/org/10.1890/15-0917.1 CrossRefGoogle Scholar
  56. Tian Q, Liu N, Bai W, Li L, Chen J, Reich PB, Yu Q, Guo DL, Smith MD, Knapp AK, Cheng WX, Lu P, Gao Y, Yang A, Wang TZ, Li X, Wang ZW, Ma YB, Han XG, Zhang WH (2016) A novel soil manganese mechanism drives plant species loss with increased nitrogen deposition in a temperate steppe. Ecology 97:65–74.  https://doi.org/10.1890/15-0917.1 CrossRefPubMedGoogle Scholar
  57. Tilman D (1993) Species richness of experimental productivity gradients: how implication is colonization limitation? Ecology 74:2179–2191.  https://doi.org/10.2307/1939572 CrossRefGoogle Scholar
  58. Turnbull LA, Crawley MJ, Rees M (2000) Are plant populations seed-limited? A review of seed sowing experiments. Oikos 88:225–238.  https://doi.org/10.1034/j.1600-0706.2000.880201.x CrossRefGoogle Scholar
  59. VanderWeide BL, Hartnett DC (2015) Belowground bud bank response to grazing under severe, short-term drought. Oecologia 178:795–806.  https://doi.org/10.1007/s00442-015-3249-y CrossRefPubMedGoogle Scholar
  60. Wan C, Sosebee RE (2000) Central dieback of the dryland bunchgrass Eragrostis curvula (weeping lovegrass) re-examined: the experimental clearance of tussock centres. J Arid Environ 46:69–78.  https://doi.org/10.1006/jare.2000.0654 CrossRefGoogle Scholar
  61. Zhang Y, Zheng L, Liu X, Jickells T, Cape JN, Goulding K et al (2008) Evidence for organic N deposition and its anthropogenic sources in China. Atmos Environ 42:1035–1041.  https://doi.org/10.1016/j.atmosenv.2007.12.015 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Key Laboratory of Tibetan Medicine Research, Northwest Institute of Plateau Biology, The Chinese Academy of SciencesXinningChina
  2. 2.State Key Laboratory of Vegetation and Environmental Change, Institute of Botany, The Chinese Academy of SciencesBeijingChina
  3. 3.College of Resource and Environment, University of Chinese Academy of SciencesBeijingChina
  4. 4.Inner Mongolia Research Center for Prataculture, Chinese Academy of SciencesBeijingChina

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