, Volume 32, Issue 3, pp 835–846 | Cite as

Non-structural carbon, nitrogen, and phosphorus between black locust and chinese pine plantations along a precipitation gradient on the Loess Plateau, China

  • Yang Cao
  • Yanan Li
  • Yunming ChenEmail author
Original Article


Key message

No soil nutrient differences between two plantations. In contrast to NSC, N and P concentrations were greater in black locust than in Chinese pine. NSC negatively, N and P positively related to precipitation for both plantations.


Precipitation is a key environmental factor affecting carbon (C), nitrogen (N), and phosphorus (P) status of plants and soils, especially in water-limited regions. However, there are potential differences among species in their sensitivity to C, N, and P in relation to variation in precipitation. We presented paired measurements of non-structural carbon (NSC), N, and P concentrations in plantations of N-fixing black locust (Robinia pseudoacacia L.) and coniferous Chinese pine (Pinus tabulaeformis Carrière) along a mean annual precipitation gradient on the Loess Plateau, China. The results showed that soil nutrients positively related to precipitation, but their differences between two plantations were not clearly visible. NSC concentrations of tree tissues were significantly greater in Chinese pine than in black locust. In contrast, the N and P concentrations and the N:P ratios were significantly greater in black locust than in Chinese pine. Leaves contained the highest N and P concentrations, whereas coarse roots contained the highest NSC concentrations. The lowest concentrations of NSC were in the stem wood. NSC concentrations were negatively related to precipitation, while N and P concentrations were positively related to precipitation for both tree plantations. The constant leaf N:P ratios indicated that the growth of Chinese pine was limited by the soil N supply, whereas black locust was limited by P. These results indicate that inherent physiological and biological processes differ with tree species, and when coupled with environmental conditions, influence the variations of C, N, and P in plant tissues to adaptation and resilience under drought stress.


Drought Plant stoichiometry Precipitation Starch Sugar 



This research was supported by the National Nature Science Foundation of China (Nos. 41201088 and 41771556), and National Key R&D Program of China (2016YFC0501703 and 2017YFC0504605), and CAS “Light of West China” Program (XAB201702). The authors would like to acknowledge the contributions made by Christian J. Rivera (Princeton University, USA) regarding the English language revision of the manuscript.

Author contribution statement

YC and YC designed the experiments. YC and YL carried out the experiments. YC wrote the manuscript with contributions from YL and YC.

Compliance with ethical standards

Conflict of interest

There are no conflicts of interest to declare.

Supplementary material

468_2018_1676_MOESM1_ESM.tif (55.2 mb)
Fig. S1. Sugars concentrations in leaves (a), branches (b), stem wood (c), bark (d), fine roots, (e) and coarse roots (f) for black locust and Chinese pine stands along a precipitation gradient on Loess Plateau. Error bars indicate the standard errors (n=3). * indicate significant differences between black locust and Chinese pine stands at each site. The different uppercase and lowercase letters indicate significant differences among sites for black locust and Chinese pine stands, respectively. Only significant regression models are displayed. (TIF 56527 KB)
468_2018_1676_MOESM2_ESM.tif (54.9 mb)
Fig. S2. Starch concentrations in leaves (a), branches (b), stem wood (c), bark (d), fine roots, (e) and coarse roots (f) for black locust and Chinese pine stands along a precipitation gradient on Loess Plateau. Error bars indicate the standard errors (n=3). * indicate significant differences between black locust and Chinese pine stands. The different uppercase and lowercase letters indicate significant differences along a precipitation gradient for black locust and Chinese pine stands, respectively. Only significant regression models are displayed. (TIF 56267 KB)


  1. Anderegg WRL (2012) Complex aspen forest carbon and root dynamics during drought A letter. Clim Change 111:983–991CrossRefGoogle Scholar
  2. Anderegg WRL, Anderegg LDL (2013) Hydraulic and carbohydrate changes in experimental drought-induced mortality of saplings in two conifer species. Tree Physiol 33:252–260CrossRefPubMedGoogle Scholar
  3. Anderegg WRL, Berry JA, Smith DD, Sperry JS, Anderegg LDL, Field CB (2012) The roles of hydraulic and carbon stress in a widespread climate-induced forest die-off. Proc Natl Acad Sci 109:233–237CrossRefPubMedGoogle Scholar
  4. Aranibar JN, Otter L, Macko SA, Feral CJW, Epstein HE, Dowty PR, Eckardt F, Shugart HH, Swap RJ (2004) Nitrogen cycling in the soil-plant system along a precipitation gradient in the Kalahari sands. Global Change Biol 10:359–373CrossRefGoogle Scholar
  5. Austin AT, Vitousek PM (1998) Nutrient dynamics on a precipitation gradient in Hawai’i. Oecologia 113:519–529CrossRefPubMedGoogle Scholar
  6. Barbaroux C, Breda N, Dufrene E (2003) Distribution of above-ground and below-ground carbohydrate reserves in adult trees of two contrasting broad-leaved species (Quercus petraea and Fagus sylvatica). New Phytol 157:605–615CrossRefGoogle Scholar
  7. Bellasio C, Fini A, Ferrini F (2014) Evaluation of a high throughput starch analysis optimised for wood. PLoS One 9:e86645CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bert D, Danjon F (2006) Carbon concentration variations in the roots, stem and crown of mature Pinus pinaster (Ait.). For Ecol Manage 222:279–295CrossRefGoogle Scholar
  9. Boldingh H, Smith GS, Klages K (2000) Seasonal concentrations of non-structural carbohydrates of five Actinidia species in fruit, leaf and fine root tissue. Ann Bot 85:469–476CrossRefGoogle Scholar
  10. Bonan GB (2008) Forests and climate change: Forcings, feedbacks, and the climate benefits of forests. Science 320:1444–1449CrossRefPubMedGoogle Scholar
  11. Bremner J, Mulvaney C (1982) Nitrogen-total. Methods of soil analysis. Part 2. Chemical and microbiological properties, pp 595–624Google Scholar
  12. Cao Y, Chen YM (2017) Coupling of plant and soil C:N:P stoichiometry in black locust (Robinia pseudoacacia) plantations on the Loess Plateau, China. Trees-Struct Funct 31:1559–1570CrossRefGoogle Scholar
  13. Chantuma P, Lacointe A, Kasemsap P, Thanisawanyangkura S, Gohet E, Clement A, Guilliot A, Ameglio T, Thaler P (2009) Carbohydrate storage in wood and bark of rubber trees submitted to different level of C demand induced by latex tapping. Tree Physiol 29:1021–1031CrossRefPubMedGoogle Scholar
  14. Chen HS, Shao MG, Li YY (2008) Soil desiccation in the Loess Plateau of China. Geoderma 143:91–100CrossRefGoogle Scholar
  15. Cierjacks A, Kowarik I, Joshi J, Hempel S, Ristow M, von der Lippe M, Weber E (2013) Biological flora of the british isles: robinia pseudoacacia. J Ecol 101:1623–1640CrossRefGoogle Scholar
  16. Cramer MD, Hawkins HJ, Verboom GA (2009) The importance of nutritional regulation of plant water flux. Oecologia 161:15–24CrossRefPubMedGoogle Scholar
  17. Deans JD, Diagne O, Lindley DK, Dione M, Parkinson JA (1999) Nutrient and organic-matter accumulation in Acacia senegal fallows over 18 years. For Ecol Manage 124:153–167CrossRefGoogle Scholar
  18. Dietze MC, Sala A, Carbone MS, Czimczik CI, Mantooth JA, Richardson AD, Vargas R (2014) Nonstructural carbon in woody plants. Annu Rev Plant Biol 65 65:667–687CrossRefPubMedGoogle Scholar
  19. Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA (2009) Plant drought stress: effects, mechanisms and management. Agron Sustain Dev 29:185–212CrossRefGoogle Scholar
  20. Gruber A, Pirkebner D, Florian C, Oberhuber W (2012) No evidence for depletion of carbohydrate pools in Scots pine (Pinus sylvestris L.) under drought stress. Plant Biol 14:142–148PubMedGoogle Scholar
  21. Han WX, Fang JY, Guo DL, Zhang Y (2005) Leaf nitrogen and phosphorus stoichiometry across 753 terrestrial plant species in China. New Phytol 168:377–385CrossRefPubMedGoogle Scholar
  22. He M, Dijkstra FA (2014) Drought effect on plant nitrogen and phosphorus: a meta-analysis. New Phytol 204:924–931CrossRefPubMedGoogle Scholar
  23. Hoch G, Richter A, Korner C (2003) Non-structural carbon compounds in temperate forest trees. Plant Cell Environ 26:1067–1081CrossRefGoogle Scholar
  24. Killingbeck KT (1996) Nutrients in senesced leaves: Keys to the search for potential resorption and resorption proficiency. Ecology 77:1716–1727CrossRefGoogle Scholar
  25. Körner C (2003) Carbon limitation in trees. J Ecol 91:4–17CrossRefGoogle Scholar
  26. Kozlowski TT (1992) Carbohydrate sources and sinks in woody-plants. Bot Rev 58:107–222CrossRefGoogle Scholar
  27. Kreuzwieser J, Gessler A (2010) Global climate change and tree nutrition: influence of water availability. Tree Physiol 30:1221–1234CrossRefPubMedGoogle Scholar
  28. Li H, Li J, He YL, Li SJ, Liang ZS, Peng CH, Polle A, Luo ZB (2013a) Changes in carbon, nutrients and stoichiometric relations under different soil depths, plant tissues and ages in black locust plantations. Acta Physiol Plant 35:2951–2964CrossRefGoogle Scholar
  29. Li MH, Cherubini P, Dobbertin M, Arend M, Xiao WF, Rigling A (2013b) Responses of leaf nitrogen and mobile carbohydrates in different Quercus species/provenances to moderate climate changes. Plant Biol 15:177–184CrossRefPubMedGoogle Scholar
  30. Li XW, Sun K, Li FY (2014) Variation in leaf nitrogen and phosphorus stoichiometry in the nitrogen-fixing Chinese sea-buckthorn (Hippophae rhamnoides L. subsp sinensis Rousi) across northern China. Ecol Res 29:723–731CrossRefGoogle Scholar
  31. Locosselli GM, Buckeridge MS (2017) Dendrobiochemistry, a missing link to further understand carbon allocation during growth and decline of trees. Trees-Struct Funct 31:1745–1758CrossRefGoogle Scholar
  32. Luttge U (2017) From dendrochronology and dendroclimatology to dendrobiochemistry. Trees-Struct Funct 31:1743–1744CrossRefGoogle Scholar
  33. Macedo MO, Resende AS, Garcia PC, Boddey RM, Jantalia CP, Urquiaga S, Campello EFC, Franco AA (2008) Changes in soil C and N stocks and nutrient dynamics 13 years after recovery of degraded land using leguminous nitrogen-fixing trees. For Ecol Manage 255:1516–1524CrossRefGoogle Scholar
  34. Matzek V, Vitousek PM (2009) N: P stoichiometry and protein : RNA ratios in vascular plants: an evaluation of the growth-rate hypothesis. Ecol Lett 12:765–771CrossRefPubMedGoogle Scholar
  35. McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut J, Sperry J, West A, Williams DG, Yepez EA (2008) Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol. 178:pp 719–739CrossRefPubMedGoogle Scholar
  36. Meier IC, Leuschner C (2014) Nutrient dynamics along a precipitation gradient in European beech forests. Biogeochemistry 120:51–69CrossRefGoogle Scholar
  37. Michelot A, Simard S, Rathgeber C, Dufrêne E, Damesin C (2012) Comparing the intra-annual wood formation of three European species (Fagus sylvatica, Quercus petraea and Pinus sylvestris) as related to leaf phenology and non-structural carbohydrate dynamics. Tree Physiol 32:1033–1045CrossRefPubMedGoogle Scholar
  38. Miller AJ, Schuur EAG, Chadwick OA (2001) Redox control of phosphorus pools in Hawaiian montane forest soils. Geoderma 102:219–237CrossRefGoogle Scholar
  39. O’Brien MJ, Leuzinger S, Philipson CD, Tay J, Hector A (2014) Drought survival of tropical tree seedlings enhanced by non-structural carbohydrate levels. Nat Clim Change 4:710–714CrossRefGoogle Scholar
  40. O’Brien MJ, Burslem DFRP., Caduff A, Tay J, Hector A (2015) Contrasting nonstructural carbohydrate dynamics of tropical tree seedlings under water deficit and variability. New Phytol 205:1083–1094CrossRefPubMedGoogle Scholar
  41. Olsen S, Cole C, Watanabe F, Dean L (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. Circular 939. Washington, DC, USDAGoogle Scholar
  42. Ordonez JC, van Bodegom PM, Witte JPM, Wright IJ, Reich PB, Aerts R (2009) A global study of relationships between leaf traits, climate and soil measures of nutrient fertility. Global Ecol Biogeogr 18:137–149CrossRefGoogle Scholar
  43. Osaki M, Shinano T, Tadano T (1991) Redistribution of carbon and nitrogen compounds from the shoot to the harvesting organs during maturation in field crops. Soil Sci Plant Nutr 37:117–128CrossRefGoogle Scholar
  44. Parkinson J, Allen S (1975) A wet oxidation procedure suitable for the determination of nitrogen and mineral nutrients in biological material. Commun Soil Sci Plant Anal 6:1–11CrossRefGoogle Scholar
  45. Qiu LP, Zhang XC, Cheng JM, Yin XQ (2010) Effects of black locust (Robinia pseudoacacia) on soil properties in the loessial gully region of the Loess Plateau, China. Plant Soil 332:207–217CrossRefGoogle Scholar
  46. Reef R, Ball MC, Feller IC, Lovelock CE (2010) Relationships among RNA: DNA ratio, growth and elemental stoichiometry in mangrove trees. Funct Ecol 24:1064–1072CrossRefGoogle Scholar
  47. Rice SK, Westerman B, Federici R (2004) Impacts of the exotic, nitrogen-fixing black locust (Robinia pseudoacacia) on nitrogen-cycling in a pine-oak ecosystem. Plant Ecol 174:97–107CrossRefGoogle Scholar
  48. Richardson AD, Carbone MS, Keenan TF, Czimczik CI, Hollinger DY, Murakami P, Schaberg PG, Xu XM (2013) Seasonal dynamics and age of stemwood nonstructural carbohydrates in temperate forest trees. New Phytol 197:850–861CrossRefPubMedGoogle Scholar
  49. Richardson AD, Carbone MS, Huggett BA, Furze ME, Czimczik CI, Walker JC, Xu XM, Schaberg PG, Murakami P (2015) Distribution and mixing of old and new nonstructural carbon in two temperate trees. New Phytol 206:590–597CrossRefPubMedPubMedCentralGoogle Scholar
  50. Ryan MG (2011) Tree responses to drought. Tree Physiol 31:237–239CrossRefPubMedGoogle Scholar
  51. Sala A, Hoch G (2009) Height-related growth declines in ponderosa pine are not due to carbon limitation. Plant Cell Environ 32:22–30CrossRefPubMedGoogle Scholar
  52. Sala A, Piper F, Hoch G (2010) Physiological mechanisms of drought-induced tree mortality are far from being resolved. New Phytol 186:274–281CrossRefPubMedGoogle Scholar
  53. Sala A, Woodruff DR, Meinzer FC (2012) Carbon dynamics in trees: feast or famine? Tree Physiol 32:764–775CrossRefPubMedGoogle Scholar
  54. Santiago LS, Kitajima K, Wright SJ, Mulkey SS (2004) Coordinated changes in photosynthesis, water relations and leaf nutritional traits of canopy trees along a precipitation gradient in lowland tropical forest. Oecologia 139:495–502CrossRefPubMedGoogle Scholar
  55. Sardans J, Penuelas J (2007) Drought changes phosphorus and potassium accumulation patterns in an evergreen Mediterranean forest. Funct Ecol 21:191–201CrossRefGoogle Scholar
  56. Sardans J, Penuelas J (2012) The role of plants in the effects of global change on nutrient availability and stoichiometry in the plant-soil system. Plant Physiol 160:1741–1761CrossRefPubMedPubMedCentralGoogle Scholar
  57. Sardans J, Rivas-Ubach A, Penuelas J (2011) Factors affecting nutrient concentration and stoichiometry of forest trees in Catalonia (NE Spain). For Ecol Manage 262:2024–2034CrossRefGoogle Scholar
  58. Sardans J, Rivas-Ubach A, Estiarte M, Ogaya R, Penuelas J (2013) Field-simulated droughts affect elemental leaf stoichiometry in Mediterranean forests and shrublands. Acta Oecolog-Int J Ecol 50:20–31CrossRefGoogle Scholar
  59. Sayer MAS, Haywood JD (2006) Fine root production and carbohydrate concentrations of mature longleaf pine (Pinus palustris P. Mill.) as affected by season of prescribed fire and drought. Trees-Structure Function 20:165–175CrossRefGoogle Scholar
  60. Shan C, Liang Z, Hao W (2002) Review on growth of locust and soil water in Loess Plateau. Acta Bot Boreali-Occident Sinica 23:1341–1346Google Scholar
  61. Tateno R, Tokuchi N, Yamanaka N, Du S, Otsuki K, Shimamura T, Xue Z, Wang S, Hou Q (2007) Comparison of litterfall production and leaf litter decomposition between an exotic black locust plantation and an indigenous oak forest near Yan’an on the Loess Plateau, China. For Ecol Manage 241:84–90CrossRefGoogle Scholar
  62. Thomas SC, Martin AR (2012) Carbon content of tree tissues: a synthesis. Forests 3:332–352CrossRefGoogle Scholar
  63. Townsend AR, Cleveland CC, Asner GP, Bustamante MMC (2007) Controls over foliar N: P ratios in tropical rain forests. Ecology 88:107–118CrossRefPubMedGoogle Scholar
  64. Tsunekawa A, Liu G, Yamanaka N, Du S (2014) Restoration and Development of the Degraded Loess Plateau, China. Springer, New YorkCrossRefGoogle Scholar
  65. Uselman SM, Qualls RG, Thomas RB (2000) Effects of increased atmospheric CO2, temperature, and soil N availability on root exudation of dissolved organic carbon by a N-fixing tree (Robinia pseudoacacia L.). Plant Soil 222:191–202CrossRefGoogle Scholar
  66. 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
  67. Villar-Salvador P, Uscola M, Jacobs DF (2015) The role of stored carbohydrates and nitrogen in the growth and stress tolerance of planted forest trees. New Forest 46(5–6):813–839CrossRefGoogle Scholar
  68. Vitousek PM, Turner DR, Kitayama K (1995) Foliar Nutrients during long-term soil development in Hawaiian montane rain-forest. Ecology 76:712–720CrossRefGoogle Scholar
  69. Wang FM, Li ZA, Xia HP, Zou B, Li NY, Liu J, Zhu WX (2010) Effects of nitrogen-fixing and non-nitrogen-fixing tree species on soil properties and nitrogen transformation during forest restoration in southern China. Soil Sci Plant Nutr 56:297–306CrossRefGoogle Scholar
  70. Wang YQ, Shao MA, Zhu YJ, Liu ZP (2011) Impacts of land use and plant characteristics on dried soil layers in different climatic regions on the Loess Plateau of China. Agric For Meteorol 151:437–448CrossRefGoogle Scholar
  71. Woodruff DR, Meinzer FC (2011) Water stress, shoot growth and storage of non-structural carbohydrates along a tree height gradient in a tall conifer. Plant Cell Environ 34:1920–1930CrossRefPubMedGoogle Scholar
  72. Woodruff DR, Meinzer FC, Marias DE, Sevanto S, Jenkins MW, McDowell NG (2015) Linking nonstructural carbohydrate dynamics to gas exchange and leaf hydraulic behavior in Pinus edulis and Juniperus monosperma. New Phytol 206:411–421CrossRefPubMedGoogle Scholar
  73. Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas ML, Niinemets U, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004) The worldwide leaf economics spectrum. Nature 428:821–827CrossRefPubMedGoogle Scholar
  74. Würth MKR, Peláez-Riedl S, Wright SJ, Körner C (2005) Non-structural carbohydrate pools in a tropical forest. Oecologia 143:11–24CrossRefPubMedGoogle Scholar
  75. Yemm E, Willis A (1954) The estimation of carbohydrates in plant extracts by anthrone. Biochem J 57:508–514CrossRefPubMedPubMedCentralGoogle Scholar
  76. Yuan ZYY, Chen HYH (2009) Global trends in senesced-leaf nitrogen and phosphorus. Global Ecol Biogeogr 18:532–542CrossRefGoogle Scholar
  77. Yuan ZY, Chen HY (2015) Decoupling of nitrogen and phosphorus in terrestrial plants associated with global changes. Nat Clim Change 5(5):465CrossRefGoogle Scholar
  78. Zhang C, Tian H, Liu J, Wang S, Liu M, Pan S, Shi X (2005) Pools and distributions of soil phosphorus in China. Global Biogeochem Cycles 19:GB1020. CrossRefGoogle Scholar
  79. Zhang JT, Ru WM, Li B (2006) Relationships between vegetation and climate on the Loess Plateau in China. Folia Geobotanica 41:151–163CrossRefGoogle Scholar
  80. Zhang H, Wu H, Yu Q, Wang Z, Wei C, Long M, Kattge J, Smith M, Han X (2013) Sampling date, leaf age and root size: implications for the study of plant C: N: P stoichiometry. PLoS One 8(4):e60360CrossRefPubMedPubMedCentralGoogle Scholar
  81. Zhang HY, Wang CK, Wang XC (2014) Spatial variations in non-structural carbohydrates in stems of twelve temperate tree species. Trees-Struct Funct 28:77–89CrossRefGoogle Scholar
  82. Zhang T, Cao Y, Chen Y, Liu G (2015) Non-structural carbohydrate dynamics in Robinia pseudoacacia saplings under three levels of continuous drought stress. Trees 29(6):1837–1849CrossRefGoogle Scholar
  83. Zhang G, Zhang P, Peng S, Chen Y, Cao Y (2017) The coupling of leaf, litter, and soil nutrients in warm temperate forests in northwestern China. Sci Rep 7(1):11754CrossRefPubMedPubMedCentralGoogle Scholar
  84. Zheng S, Shangguan Z (2007) Spatial patterns of leaf nutrient traits of the plants in the Loess Plateau of China. Trees-Struct Funct 21:357–370CrossRefGoogle Scholar
  85. Zhou XH, Talley M, Luo YQ (2009) Biomass, litter, and soil respiration along a precipitation gradient in Southern Great Plains, USA. Ecosystems 12:1369–1380CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  1. 1.State Key Laboratory of Soil Erosion and Dryland Farming on the Loess PlateauNorthwest A&F UniversityYanglingChina
  2. 2.Institute of Soil and Water ConservationChinese Academy of Sciences and Ministry of Water ResourcesYanglingChina
  3. 3.College of ForestryNorthwest A&F UniversityYanglingChina

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