Plant and Soil

, Volume 428, Issue 1–2, pp 291–305 | Cite as

Unravelling community assemblages through multi-element stoichiometry in plant leaves and roots across primary successional stages in a glacier retreat area

  • Yonglei Jiang
  • Mengya Song
  • Sheng Zhang
  • Zhiquan Cai
  • Yanbao LeiEmail author
Regular Article


Background and aims

Our understandings on the patterns and mechanisms of plant community assembly during succession, especially the primary succession in glacier retreat areas, remain limited. The Hailuogou Glacier Chronosequence provides a distinctive place to disentangle the biotic interactions and abiotic filtering effects on community successional trajectories.


Through community-weighted approaches, we quantified elements allocation and regulation in leaves and roots, N:P stoichiometry, and the biotic and abiotic controls guiding community dynamics along the 120-year chronosequence.


Across seven primary successional stages, plant leaves featured higher concentrations of macro-elements with lower coefficients of variation (CV) with increasing succession; whereas, fine roots contained more micro-elements with higher CV. From the early to late stages, foliar N:P increased linearly from 8.2 to 20.1.


These findings highlighted that the limiting factor for plant growth shifted from N to P over one century of deglaciation. Edaphic factors (pH, bulk density, N and P concentrations) acted as deterministic filtering for trait convergence in the early stages, while biotic factors (species richness and plant litter biomass) for competitive exclusion dominated the late stages hosting species with stronger homoeostatic regulation and more conservative nutrient use.


Edaphic and biotic drivers Hailuogou Glacier Chronosequence Elements homoeostatic regulation Plant community assembly 



The authors are grateful to the Gongga Mountain Alpine Ecosystem Observation Station, Chinese Academy of Sciences for logistic support. This work was supported by the National Science Foundation of China (Nos. 31570598 and 31370607), the Talent Program of Hangzhou Normal University (2016QDL020) and the Frontier Science Key Research Programs of Chinese Academy of Sciences (QYZDB-SSW-DQC037). The authors also thank LetPub ( for its linguistic assistance during the preparation of this manuscript.

Supplementary material

11104_2018_3683_MOESM1_ESM.docx (761 kb)
ESM 1 (DOCX 760 kb)


  1. Achat DL, Bakker MR, Zeller B, Pellerin S, Bienaimé S, Morel C (2010) Long-term organic phosphorus mineralization in Spodosols under forests and its relation to carbon and nitrogen mineralization. Soil Biol Biochem 42(9):1479–1490. CrossRefGoogle Scholar
  2. Aerts R, Chapin FS (2000) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. In: Fitter AH, Raffaelli DG (eds) Advances in ecological research, 30, 1–67. Google Scholar
  3. Arroyo-Rodríguez V, Melo FPL, Martinez-Ramos M, Bongers F, Chazdon RL, Meave JA, Norden N, Santos BA, Leal IR, Tabarelli M (2017) Multiple successional pathways in human-modified tropical landscapes: new insights from forest succession, forest fragmentation and landscape ecology research. Biol Rev 92:326–340. CrossRefPubMedGoogle Scholar
  4. Bergholz K, May F, Giladi I, Ristow M, Ziv Y, Jeltsch F (2017) Environmental heterogeneity drives fine-scale species assembly and functional diversity of annual plants in a semi-arid environment. Perspec Plant Ecol 24:138–146. CrossRefGoogle Scholar
  5. Botta-Dukát Z, Czúcz B (2016) Testing the ability of functional diversity indices to detect trait convergence and divergence using individual-based simulation. Methods Ecol Evol 7:114–126. CrossRefGoogle Scholar
  6. Callaway RM, Brooker RW, Choler P, Kikvidze Z, Lortie CJ, Michalet R, Paolini L, Pugnaire FI, Newingham B, Aschehoug ET, Armas C, Kikodze D, Cook BJ (2002) Positive interactions among alpine plants increase with stress. Nature 417:844–848. CrossRefGoogle Scholar
  7. Cavagnaro TR, Jackson LE, Six J, Ferris H, Goyal S, Asami D, Scow KM (2006) Arbuscular mycorrhizas, microbial communities, nutrient availability, and soil aggregates in organic tomato production. Plant Soil 282:209–225. CrossRefGoogle Scholar
  8. Chamberlain SA, Bronstein JL, Rudgers JA (2014) How context dependent are species interactions? Ecol Lett 17:881–890. CrossRefPubMedGoogle Scholar
  9. Craine JM, Morrow C, Stock WD (2008) Nutrient concentration ratios and co-limitation in South African grasslands. New Phytol 179:829–836. CrossRefPubMedGoogle Scholar
  10. Craine JM, Brookshire ENJ, Cramer MD, Hasselquist NJ, Koba K, Marin-Spiotta E, Wang LX (2015) Ecological interpretations of nitrogen isotope ratios of terrestrial plants and soils. Plant Soil 396:1–26. CrossRefGoogle Scholar
  11. Curtis JT, McIntosh RP (1951) An upland forest continuum in the prairie-forest border region of Wisconsin. Ecology 32:476–496. CrossRefGoogle Scholar
  12. Elser JJ, Bracken MES, Cleland EE, Gruner DS, Harpole WS, Hillebrand H, Ngai JT, Seabloom EW, Shurin JB, Smith JE (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10:1135–1142. CrossRefPubMedGoogle Scholar
  13. Garnier E, Cortez J, Billès G, Navas ML, Roumet C, Debussche M, Laurent G, Blanchard A, Aubry D, Bellmann A, Neill C, Toussaint JP (2004) Plant functional markers capture ecosystem properties during secondary succession. Ecology 85:2630–2637. CrossRefGoogle Scholar
  14. Gei MG, Powers JS (2013) Do legumes and non-legumes tree species affect soil properties in unmanaged forests and plantations in Costa Rican dry forests? Soil Biol Biochem 57:264–272. CrossRefGoogle Scholar
  15. Goodale C (2017) Multiyear fate of a 15N tracer in a mixed deciduous forest: retention, redistribution, and differences by mycorrhizal association. Glob Chang Biol 23:867–880. CrossRefPubMedGoogle Scholar
  16. Guo WQ, Liu SY, Xu JL, Wu LZ, Shangguan DH, Yao XJ, Wei JF, Bao WJ, Yu PC, Liu Q, Jiang ZL (2015) The second Chinese glacier inventory: data, methods and results. J Glaciol 61:357–372. CrossRefGoogle Scholar
  17. Güsewell S (2004) N:P ratios in terrestrial plants: variation and functional significance. New Phytol 164:243–266. CrossRefGoogle Scholar
  18. Han W, Fang J, Reich PB, Ian Woodward F, Wang Z (2011) Biogeography and variability of eleven mineral elements in plant leaves across gradients of climate, soil and plant functional type in China. Ecol Lett 14:788–796. CrossRefPubMedGoogle Scholar
  19. He M, Dijkstra FA, Zhang K, Tan H, Zhao Y, Li X (2016) Influence of life form, taxonomy, climate, and soil properties on shoot and root concentrations of 11 elements in herbaceous plants in a temperate desert. Plant Soil 398:339–350. CrossRefGoogle Scholar
  20. Hooper D, Coughlan J, Mullen M (2008) Structural equation modelling: guidelines for determining model fit. Electron J Bus Res Methods 6:53–60Google Scholar
  21. Jeyasingh PD, Weider LJ, Sterner RW (2009) Genetically-based trade-offs in response to stoichiometric food quality influence competition in a keystone aquatic herbivore. Ecol Lett 12:1229–1237. CrossRefPubMedGoogle Scholar
  22. Jiang Y, Lei Y, Yang Y, Korpelainen H, Niinemets Ü, Li C (2018) Divergent assemblage patterns and driving forces for bacterial and fungal communities along a glacier forefield chronosequence. Soil Biol Biochem 118:207–216. CrossRefGoogle Scholar
  23. Karimi R, Folt CL (2006) Beyond macronutrients: element variability and multielement stoichiometry in freshwater invertebrates. Ecol Lett 9:1273–1283. CrossRefPubMedGoogle Scholar
  24. Lambers H, Raven JA, Shaver GR, Smith SE (2008) Plant nutrient acquisition strategies change with soil age. Trends Ecol Evol 23:95–103. CrossRefPubMedGoogle Scholar
  25. Lei Y, Zhou J, Xiao H, Duan B, Wu Y, Korpelainen H, Li C (2015) Soil nematode assemblages as bioindicators of primary succession along a 120-year-old chronosequence on the Hailuogou Glacier forefield, SW China. Soil Biol Biochem 88:362–371. CrossRefGoogle Scholar
  26. Lohbeck M, Poorter L, MartiNez-Ramos M, Bongers F (2015) Biomass is the main driver of changes in ecosystem process rates during tropical forest succession. Ecology 96:1242–1252. CrossRefGoogle Scholar
  27. Mariotte P, Canarini A, Dijkstra FA (2017) Stoichiometric N:P flexibility and mycorrhizal symbiosis favour plant resistance against drought. J Ecol 105:958–967. CrossRefGoogle Scholar
  28. Metali F, Salim KA, Burslem DFRP (2012) Evidence of foliar aluminium accumulation in local, regional and global datasets of wild plants. New Phytol 193:637–649. CrossRefPubMedGoogle Scholar
  29. Miatto RC, Wright IJ, Batalha MA (2016) Relationships between soil nutrient status and nutrient-related leaf traits in Brazilian cerrado and seasonal forest communities. Plant Soil 404:13–33. CrossRefGoogle Scholar
  30. Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–66CrossRefGoogle Scholar
  31. Nelson DW, Sommers LE (1982) Total carbon, organic carbon and organic matter. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis. American Society of Agronomy, Madison, pp 539–579Google Scholar
  32. Niinemets U, Kull K (2005) Co-limitation of plant primary productivity by nitrogen and phosphorus in a species-rich wooded meadow on calcareous soils. Acta Oecol 28:345–356. CrossRefGoogle Scholar
  33. Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos PS, Stevens MH, Szoecs E, Wagner H (2016) Package ‘vegan’.
  34. Ostonen I, Truu M, Helmisaari H, Lukac M, Borken W, Vanguelova E, Godbold DL, Lohmus K, Zang U, Tedersoo L, Preem JK, Rosenvald K, Aosaar J, Armolaitis K, Frey J, Kabral N, Kukumägi M, Leppälammi-Kujansuu J, Lindroos AJ, Merilä P, Napa U, Njöd P, Parts K, Uri V, Varik M, Truu J (2017) Adaptive root foraging strategies along a boreal–temperate forest gradient. New Phytol 215:977–991. CrossRefPubMedGoogle Scholar
  35. Pavoine S, Vela E, Gachet S, de Belair G, Bonsall MB (2011) Linking patterns in phylogeny, traits, abiotic variables and space: a novel approach to linking environmental filtering and plant community assembly. J Ecol 99:165–175. CrossRefGoogle Scholar
  36. Peñuelas J, Sardans J, Llusia Owen S, Carnicer J, Giambelluca TW, Rezende EL, Waite M, Niinemets Ü (2010) Faster returns on leaf economics and different biogeochemical niche in invasive compared with native plant species. Glob Chang Biol 16:2171–2185. CrossRefGoogle Scholar
  37. R Core Team (2013) R: a language and environment for statistical computing. R foundation for statistical computing.
  38. Rejou-Mechain M, Flores O, Pelissier R, Fayolle A, Fauvet N, Gourlet-Fleury S (2014) Tropical tree assembly depends on the interactions between successional and soil filtering processes. Glob Ecol Biogeogr 23:1440–1449. CrossRefGoogle Scholar
  39. Sardans J, Janssens IA, Alonso R, Veresoglou SD, Rillig MC, Sanders TGM, Carnicer J, Filella I, Farré-Armengol G, Peñuelas J (2015) Foliar elemental composition of European forest tree species associated with evolutionary traits and present environmental and competitive conditions. Glob Ecol Biogeogr 24:240–255. CrossRefGoogle Scholar
  40. Skeen JN (1973) An extension of the concept of importance value in analyzing forest communities. Ecology 54:655–656. CrossRefGoogle Scholar
  41. Song M, Yu L, Jiang Y, Lei Y, Korpelainen H, Niinemets Ü, Li C (2017) Nitrogen-controlled intra-and interspecific competition between Populus purdomii and Salix rehderiana drive primary succession in the Gongga Mountain glacier retreat area. Tree Physiol 37:799–814. CrossRefPubMedGoogle Scholar
  42. Sperfeld E, Wagner ND, Halvorson HM, Malishev M, Raubenheimer D (2017) Bridging ecological stoichiometry and nutritional geometry with homeostasis concepts and integrative models of organism nutrition. Funct Ecol 31:286–296. CrossRefGoogle Scholar
  43. Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, PrincetonGoogle Scholar
  44. Tessier JT, Raynal DJ (2003) Use of nitrogen to phosphorus ratios in plant tissue as an indicator of nutrient limitation and nitrogen saturation. J Appl Ecol 40:523–534. CrossRefGoogle Scholar
  45. Townsend AR, Cleveland CC, Asner GP, Bustamante MMC (2007) Controls over foliar N:P ratios in tropical rain forests. Ecology 88:107–118.[107,COFNRI]2.0.CO;2Google Scholar
  46. Vitousek PM, Menge DNL, Reed SC, Cleveland CC (2013) Biological nitrogen fixation: rates, patterns and ecological controls in terrestrial ecosystems. Philos Trans R Soc B 368:20130119. CrossRefGoogle Scholar
  47. Walker TW, Syers JK (1976) The fate of phosphorus during pedogenesis. Geoderma 15:1–19. CrossRefGoogle Scholar
  48. Wardle DA, Walker LR, Bardgett RD (2004) Ecosystem properties and forest decline in contrasting long-term chronosequences. Science 305:509–513. CrossRefGoogle Scholar
  49. Warton DI, Duursma RA, Falster DS, Taskinen S (2012) SMATR 3- an R package for estimation and inference about allometric lines. Methods Ecol Evol 3:257–259. CrossRefGoogle Scholar
  50. Weiher E, Freund D, Bunton T, Stefanski A, Lee T, Bentivenga S (2011) Advances, challenges and a developing synthesis of ecological community assembly theory. Philos Trans R Soc B 366:2403–2413. CrossRefGoogle Scholar
  51. Yang Y, Wang G, Shen H, Yang Y, Cui H, Liu Q (2014) Dynamics of carbon and nitrogen accumulation and C:N stoichiometry in a deciduous broadleaf forest of deglaciated terrain in the eastern Tibetan plateau. For Ecol Manag 312:10–18. CrossRefGoogle Scholar
  52. Yu Q, Chen Q, Elser JJ, He N, Wu H, Zhang G, Wu J, Bai Y, Han X (2010) Linking stoichiometric homoeostasis with ecosystem structure, functioning and stability. Ecol Lett 13:1390–1399. CrossRefPubMedGoogle Scholar
  53. Zemp M, Haeberli W, Hoelzle M, Paul F (2006) Alpine glaciers to disappear within decades? Geophys Res Lett 33:L13504. CrossRefGoogle Scholar
  54. Zhang W, Zhao J, Pan F, Li D, Chen H, Wang K (2015) Changes in nitrogen and phosphorus limitation during secondary succession in a karst region in southwest China. Plant Soil 391:77–91. CrossRefGoogle Scholar
  55. Zhao N, Yu GR, He NP, Wang QF, Guo DL, Zhang XY, Wang RL, Xu ZW, Jiao CC, Li NN, Jia YL (2016) Coordinated pattern of multi-element variability in leaves and roots across Chinese forest biomes. Glob Ecol Biogeogr 25:359–367. CrossRefGoogle Scholar
  56. Zhong XH, Luo J, Wu N (1997) Researches of the forest ecosystems on Gongga Mountain. Chengdu University of Science and Technology Press, ChengduGoogle Scholar
  57. Zhou J, Bing H, Wu Y, Yang Z, Wang J, Sun H, Luo J, Liang H (2016) Rapid weathering processes of a 120-year-old chronosequence in the Hailuogou Glacier foreland, Mt. Gongga, SW China. Geoderma 267:78–91. CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Yonglei Jiang
    • 1
    • 2
  • Mengya Song
    • 1
    • 2
  • Sheng Zhang
    • 1
  • Zhiquan Cai
    • 3
  • Yanbao Lei
    • 1
    Email author
  1. 1.Key Laboratory of Mountain Surface Processes and Ecological Regulation, Institute of Mountain Hazards and EnvironmentChinese Academy of SciencesChengduChina
  2. 2.University of Chinese Academy of SciencesBeijingChina
  3. 3.Key Laboratory of Tropical Plant Resources and Sustainable Use, Xishuangbanna Tropical Botanical GardenChinese Academy of SciencesMenglaChina

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