Plant and Soil

, Volume 430, Issue 1–2, pp 113–125 | Cite as

Imbalanced plant stoichiometry at contrasting geologic-derived phosphorus sites in subtropics: the role of microelements and plant functional group

  • Jiahao Wen
  • Huawei Ji
  • Ningxiao Sun
  • Huimin Tao
  • Baoming Du
  • Dafeng Hui
  • Chunjiang LiuEmail author
Regular Article


Background and Aim

Subtropical soils are generally characterized as deficient in phosphorus (P), calcium (Ca) and magnesium (Mg), but rich in iron (Fe) and aluminum (Al). However, soils developed in phosphate rock are extremely P-rich in subtropical forests, southwestern China. Factors controlling plant stoichiometric traits across variable P sites are still not clear.


We investigated leaf macroelements (C, N, P, K, Ca and Mg), microelements (Mn, Fe, Zn, and Cu), and non-essential elements (Na and Al) and their element:P ratios for 21 woody plant species at both P-rich and P-deficient sites.


Plants between the two P type sites were mainly discriminated by Mn, Al, N and their P ratios, and between functional groups by Cu, Fe, Zn and their P ratios. There were higher leaf N, P, K, Ca, Fe and Zn concentrations but lower Mn, Cu and Al at the P-rich sites. Evergreen conifers displayed strict homeostasis while evergreen and deciduous broadleaf were more plastic and had variable ratios across different nutrients.


Microelements have strong influences on plant stoichiometry to differentiate geologic-derived P sites in subtropics, and three functional group plants have adopted different stoichiometric strategies under variable nutrient conditions.


Multiple nutrients Ecological stoichiometry Phosphorus-rich soils Subtropics 



This work was financially supported by the National Key R&D Program of China (2016YFC0502501) and the National Natural Science Foundation of China (NSFC 31670626, 31270640 and 31070532). We are grateful to the support by the Instrumental Analysis Center of Shanghai Jiao Tong University. We thank Dr. Wuyuan Yin for his invaluable help in identifying tree species and anonymous reviewers for their precious comments and constructive suggestions to improve this manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11104_2018_3728_MOESM1_ESM.docx (1.5 mb)
ESM 1 (DOCX 1526 kb)


  1. Aerts R (1995) The advantages of being evergreen. Trends Ecol Evol 10:402CrossRefPubMedGoogle Scholar
  2. Ågren GI, Weih M (2012) Plant stoichiometry at different scales: element concentration patterns reflect environment more than genotype. New Phytol 194:944–952CrossRefPubMedGoogle Scholar
  3. Baxter IR, Vitek O, Lahner B, Muthukumar B, Borghi M, Morrissey J, Guerinot ML, Salt DE (2008) The leaf ionome as a multivariable system to detect a plant's physiological status. Proc Natl Acad Sci U S A 105:12081–12086Google Scholar
  4. Bhattarai KR, Vetaas OR (2003) Variation in plant species richness of different life forms along a subtropical elevation gradient in the Himalayas, East Nepal. Nepal Global Ecol Biogeogr 12:327–340CrossRefGoogle Scholar
  5. Castle S, Neff J (2009) Plant response to nutrient availability across variable bedrock geologies. Ecosystems 12:101–113CrossRefGoogle Scholar
  6. Chapin FS III (1980) The mineral nutrition of wild plants. Annu Rev Ecol Syst 11:233–260CrossRefGoogle Scholar
  7. Cronan CS, Grigal DF (1995) Use of calcium/aluminum ratios as indicators of stress in Forest ecosystems. J Environ Qual 24:209–226CrossRefGoogle Scholar
  8. Dahlquist RL, Knoll JW (1978) Inductively coupled plasma-atomic emission spectrometry: analysis of biological materials and soils for major, trace, and ultra-trace elements. Appl Spectrosc 32:1–30CrossRefGoogle Scholar
  9. Doust JL (2010) A comparative study of life history and resource allocation in selected Umbelliferae. Biol J Linn Soc 13:139–154CrossRefGoogle Scholar
  10. Ducic T, Polle A (2005) Transport and detoxification of manganese and copper in plants. Braz J Phys 17:33–38Google Scholar
  11. Elser JJ, Fagan WF, Denno RF, Dobberfuhl DR, Folarin A, Huberty A, Interlandi S, Kilham SS, McCauley E, Schulz KL, Siemann EH, Sterner RW (2000) Nutritional constraints in terrestrial and freshwater food webs. Nature 408:578–580CrossRefPubMedGoogle Scholar
  12. Garten CT (1976) Correlations between concentrations of elements in plants. Nature 261:686–688CrossRefGoogle Scholar
  13. Gerdol R, Marchesini R, Iacumin P (2016) Bedrock geology interacts with altitude in affecting leaf growth and foliar nutrient status of mountain vascular plants. J Plant Ecol: rtw092, rtw092Google Scholar
  14. Group TAP (2016) An update of the angiosperm phylogeny group classification for the orders and families of flowering plants: APG III. Bot J Linn Soc 181:1–20CrossRefGoogle Scholar
  15. Hall EK, Maixner F, Franklin O, Daims H, Richter A, Battin T (2011) Linking microbial and ecosystem ecology using ecological stoichiometry: a synthesis of conceptual and empirical approaches. Ecosystems 14:261–273CrossRefGoogle Scholar
  16. Han WX, Fang JY, Reich PB, Ian Woodward F, Wang ZH (2011) Biogeography and variability of eleven mineral elements in plant leaves across gradients of climate, soil and plant functional type in China. Ecol Lett 14:788–796CrossRefPubMedGoogle Scholar
  17. Hartmann J, Moosdorf N (2012) The new global lithological map database GLiM: a representation of rock properties at the earth surface. Geochem Geophys Geosyst 13(12)Google Scholar
  18. Hayes P, Turner BL, Lambers H, Laliberté E, Bellingham P (2013) Foliar nutrient concentrations and resorption efficiency in plants of contrasting nutrient-acquisition strategies along a 2-million-year dune chronosequence. J Ecol 102:396–410CrossRefGoogle Scholar
  19. Herbert DA, Williams M, Rastetter EB (2003) A model analysis of N and P limitation on carbon accumulation in Amazonian secondary forest after alternate land-use abandonment. Biogeochemistry 65:121–150CrossRefGoogle Scholar
  20. Jackson ML (1960) Soil chemical analysis. Agron J 85:288Google Scholar
  21. Ji H, Du B, Liu C (2017) Elemental stoichiometry and compositions of weevil larvae and two acorn hosts under natural phosphorus variation. Sci Rep 7:45810CrossRefPubMedPubMedCentralGoogle Scholar
  22. Karimi R, Folt CL (2006) Beyond macronutrients: element variability and multielement stoichiometry in freshwater invertebrates. Ecol Lett 9:1273–1283CrossRefPubMedGoogle Scholar
  23. Koerselman W, Meuleman AFM (1996) The vegetation N:P ratio: a new tool to detect the nature of nutrient limitation. J Appl Ecol 33:1441–1450CrossRefGoogle Scholar
  24. Lambers H, Hayes PE, Laliberté E, Oliveira RS, Turner BL (2015) Leaf manganese accumulation and phosphorus-acquisition efficiency. Trends Plant Sci 20:83–90CrossRefPubMedGoogle Scholar
  25. Lei Y, Korpelainen H, Li C (2007) Physiological and biochemical responses to high Mn concentrations in two contrasting Populus cathayana populations. Chemosphere 68:686–694CrossRefPubMedGoogle Scholar
  26. Liang C, Pineros MA, Tian J, Yao Z, Sun L, Liu J, Shaff J, Coluccio A, Kochian LV, Liao H (2013) Low pH, aluminum, and phosphorus coordinately regulate malate exudation through GmALMT1 to improve soybean adaptation to acid soils. Plant Physiol 161:1347–1361CrossRefPubMedPubMedCentralGoogle Scholar
  27. Lynch JP, Clair SBS (2004) Mineral stress: the missing link in understanding how global climate change will affect plants in real world soils. Field Crop Res 90:101–115CrossRefGoogle Scholar
  28. Markert B (1994) Environmental sampling for trace analysis. New YorkGoogle Scholar
  29. Mengel K, Kirkby EA, Kosegarten H, Appel T (1982) Principles of plant nutrition. Int Potash InstGoogle Scholar
  30. Millaleo R, Reyesdíaz M, Ivanov AG, Mora ML, Alberdi M (2010) Manganese as essential and toxic element for plants: transport, accumulation and resistance mechanisms. J Soil Sci Plant Nutr 10:476–494CrossRefGoogle Scholar
  31. Nally RM, Walsh CJ (2004) Hierarchical partitioning public-domain software. Biodivers Conserv 13:659–660CrossRefGoogle Scholar
  32. Oleksyn J, Reich PB, Zytkowiak R, Karolewski P, Tjoelker MG (2002) Needle nutrients in geographically diverse Pinus sylvestris L. Popul Ann For Sci 59:1–18CrossRefGoogle Scholar
  33. Palmer C, Guerinot ML (2009) A question of balance: facing the challenges of cu, Fe and Zn Homeostasis. Nat Chem Biol 5:333–340CrossRefPubMedPubMedCentralGoogle Scholar
  34. Porter WM, Robson AD, Abbott LK (1987) Field survey of the distribution of vesicular-arbuscular mycorrhizal Fungi in relation to soil pH. J Appl Ecol 24:659CrossRefGoogle Scholar
  35. Reich PB, Oleksyn J (2004) Global patterns of plant leaf N and P in relation to temperature and latitude. Proc Natl Acad Sci U S A 101:11001–11006CrossRefPubMedPubMedCentralGoogle Scholar
  36. Reich PB, Koike T, Gower ST, Schoettle AW (1995) Causes and consequences of variation in conifer leaf life-span. USA, Causes and Consequences of Variation in Conifer Leaf Life-SpanGoogle Scholar
  37. Rivas-Ubach A, Peñuelas J (2012) Strong relationship between elemental stoichiometry and metabolome in plants. Proc Natl Acad Sci U S A 109:4181–4186CrossRefPubMedPubMedCentralGoogle Scholar
  38. Schlesinger WH, Delucia EH, Billings WD (1989) Nutrient-use efficiency of Woody plants on contrasting soils in the western Great Basin, Nevada. Ecology 70:105–113CrossRefGoogle Scholar
  39. Shane MW, Lambers H (2005) Manganese accumulation in leaves of Hakea prostrata (Proteaceae) and the significance of cluster roots for micronutrient uptake as dependent on phosphorus supply. Physiol Plant 124:441–450CrossRefGoogle Scholar
  40. Shen H, Yan XL (2001) Types of aluminum toxicity and plants resistance to aluminum toxicity chin. J Soil Sci 06:281–285Google Scholar
  41. Sun QB, Shen RF, Zhao XQ, Chen RF, Dong XY (2008) Phosphorus enhances Al resistance in Al-resistant Lespedeza bicolor but not in Al-sensitive L. cuneata under relatively high Al stress. Ann Bot 102:795–804CrossRefPubMedPubMedCentralGoogle Scholar
  42. Sun X, Kang H, Kattge J, Gao Y, Liu C (2015) Biogeographic patterns of multi-element stoichiometry of Quercus varia. Can J Forest Res 45:1827–1834CrossRefGoogle Scholar
  43. Thompson K, Parkinson JA, Band SR, Spencer RE (2010) A comparative study of leaf nutrient concentrations in a regional herbaceous flora. New Phytol 136:679–689CrossRefGoogle Scholar
  44. Townsend AR, Cleveland CC, Asner GP, Bustamante MMC (2007) Controls over foliar n:p ratios in tropical rain forests. Ecology 88:107–118CrossRefPubMedGoogle Scholar
  45. Treseder KK, Vitousek PM (2001) Potential ecosystem-level effects of genetic variation among populations of Metrosideros polymorpha from a soil fertility gradient in Hawaii. Oecologia 126:266–275CrossRefPubMedGoogle Scholar
  46. Vergutz L, Manzoni S, Porporato A, Novais RF, Jackson RB (2012) Global resorption efficiencies and concentrations of carbon and nutrients in leaves of terrestrial plants. Ecol Monogr 82:205–220CrossRefGoogle Scholar
  47. Vetaas OR (1997) The effect of canopy disturbance on species richness in a central Himalayan oak Forest. Plant Ecol 132:29–38CrossRefGoogle Scholar
  48. Vitousek PM, Turner DR, Kitayama K (1995) Foliar nutrients during long-term soil development in Hawaiian montane rain Forest. Ecology 76:712–720CrossRefGoogle Scholar
  49. Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen–phosphorus interactions. Ecol Appl 20:5–15CrossRefPubMedGoogle Scholar
  50. Walker TW, Syers JK (1976) The fate of phosphorus during pedogenesis. Geoderma 15:1–19CrossRefGoogle Scholar
  51. Wrb IWG (2014) World Reference Base for soil resources 2014: international soil classification system for naming soils and creating legends for soil mapsGoogle Scholar
  52. Wu Z and Zhu Y (1987) The Vegetation of Yunnan. Science and Technology Press, BeijingGoogle Scholar
  53. Xiao G, Li T, Zhang X, Yu H, Huang H, Gupta DK (2009) Uptake and accumulation of phosphorus by dominant plant species growing in a phosphorus mining area. J Hazard Mater 171:542–550CrossRefPubMedGoogle Scholar
  54. Yan K, Fu DG, Feng H, Duan CQ (2011) Leaf nutrient stoichiometry of plants in the phosphorus-enriched soils of the Lake Dianchi watershed, southwestern China. Chin J Plant Ecol 35:353–361CrossRefGoogle Scholar
  55. Yan K, Duan C, Fu D, Li J, Wong MHG, Qian L, Tian Y (2015) Leaf nitrogen and phosphorus stoichiometry of plant communities in geochemically phosphorus-enriched soils in a subtropical mountainous region, SW China. Environ Earth Sci 74:3867–3876CrossRefGoogle Scholar
  56. Yang SX, Deng H, Li MS (2008) Manganese uptake and accumulation in a Woody Hyperaccumulator. Schima Superba Plant Soil Environ 54:441–446CrossRefGoogle Scholar
  57. Zhang SB, Zhang JL, Slik JWF, Cao KF (2012) Leaf element concentrations of terrestrial plants across China are influenced by taxonomy and the environment. Glob Ecol Biogeogr 21:809–818CrossRefGoogle Scholar
  58. Zhao N, Yu G, He N, Wang Q, Guo D, Zhang X, Wang R, Xu Z, Jiao C, Li N, Jia Y (2016) Coordinated pattern of multi-element variability in leaves and roots across Chinese forest biomes. Glob Ecol Biogeogr 25:359–367CrossRefGoogle Scholar
  59. Zhou X, Sun X, Du B, Yin S, Liu C (2015) Multielement stoichiometry in Quercus variabilis under natural phosphorus variation in subtropical China. Sci Rep 5:7839CrossRefPubMedPubMedCentralGoogle Scholar
  60. Zhu L, Zhu J, Chen Q, Zhu A (2008) The distribution law and controlling factors of the rich phosphorite ore in anning phosphorous deposit, yunnan province. Geol Resour in Chinese 01:40–44Google Scholar
  61. Zhu F, Lu X, Liu L, Mo J (2015) Phosphate addition enhanced soil inorganic nutrients to a large extent in three tropical forests. Sci Rep 5:7923CrossRefPubMedPubMedCentralGoogle Scholar

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© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.School of Agriculture and Biology and Research Centre for Low-Carbon AgricultureShanghai Jiao Tong UniversityShanghaiChina
  2. 2.Shanghai Urban Forest Research Station, State Forestry AdministrationShanghaiChina
  3. 3.Department of Biological SciencesTennessee State UniversityNashvilleUSA
  4. 4.Key Laboratory of Urban Agriculture, Ministry of AgricultureShanghaiChina

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