Journal of Mountain Science

, Volume 13, Issue 7, pp 1217–1228 | Cite as

Leaf stable carbon isotope composition in Picea schrenkiana var. tianschanica in relation to leaf physiological and morphological characteristics along an altitudinal gradient

  • Hui-wen Zhang
  • Zhen Wu
  • Hong-lang Xiao


To understand the effects of leaf physiological and morphological characteristics on δ 13C of alpine trees, we examined leaf δ 13C value, LA, SD, LNC, LPC, LKC, Chla+b, LDMC, LMA and Narea in one-year-old needles of Picea schrenkiana var. tianschanica at ten points along an altitudinal gradient from 1420 m to 2300 m a.s.l. on the northern slopes of the Tianshan Mountains in northwest China. Our results indicated that all the leaf traits differed significantly among sampling sites along the altitudinal gradient (P<0.001). LA, SD, LPC, LKC increased linearly with increasing elevation, whereas leaf δ 13C, LNC, Chla+b, LDMC, LMA and Narea varied non-linearly with changes in altitude. Stepwise multiple regression analyses showed that four controlled physiological and morphological characteristics influenced the variation of δ 13C. Among these four controlled factors, LKC was the most profound physiological factor that affected δ 13C values, LA was the secondary morphological factor, SD was the third morphological factor, LNC was the last physiological factor. This suggested that leaf δ 13C was directly controlled by physiological and morphological adjustments with changing environmental conditions due to the elevation.


Alpine trees Leaf Carbon isotope composition Physiological characteristics Morphological characteristics Altitudinal variation 

Abbreviations of leaf parameters


leaf carbon isotope composition


leaf projected area per 100 needles


stomatal density


leaf nitrogen concentration per unit mass


leaf phosphorus concentration per unit mass


leaf potassium concentration per unit mass


pigment contents


leaf dry matter content


leaf mass per unit area


leaf nitrogen concentration per unit area


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Basile B, Reidel EJ, Weinbaum SA, et al. (2003) Leaf potassium concentration, CO2 exchange and light interception in almond trees (Prunus dulcis (Mill) D.A. Webb). Scientia Horticulturae 98(2): 185–194. DOI: 10.1016/S0304-4238(02)00214-5CrossRefGoogle Scholar
  2. Bednarz CW, Oosterhuis DM, Evans RD (1998) Leaf photosynthesis and carbon isotope discrimination of cotton in response to potassium deficiency. Environmental and Experimental Botany 39(2): 131–139. DOI: 10.1016/S0098-8472(97)00039-7CrossRefGoogle Scholar
  3. Beerling DJ, Mattey DP, Ghaloner WG (1993) Shifts in the 813C composition of Salix herbacea L. leaves in response to spatial and temporal gradients of atmospheric CO2 concentration. Proceedings of the Royal Society B: Biological Sciences 253(1336): 53–60. DOI: 10.1098/rspb.1993.0081CrossRefGoogle Scholar
  4. Chen T, Qin DH, Li JF, et al. (2000) Study on climatic significance of fir tree-ring δ 13C from Zhaosu County of Xinjiang Region, China. Journal of Glaciology and Geocryology 22(4): 347–352. DOI: 10.3969/j.issn.1000-0240.2000.04.009 (in Chinese)Google Scholar
  5. Cordell S, Goldstein G, Mueller-Dombois D, et al. (1998) Physiological and morphological variation in Metrosideros polymorpha, a dominant Hawaiian tree species, along an altitudinal gradient: role of phenotypic plasticity. Oecologia 113(2): 188–196. DOI: 10.1007/s004420050367CrossRefGoogle Scholar
  6. Cordell S, Goldstein G, Meinzer FC, et al. (1999) Allocation of nitrogen and carbon in leaves of Metrosideros polymorpha regulates carboxylation capacity and δ 13C along an altitudinal gradient. Functional Ecology 13(6): 811–818. DOI: 10.1046/j.1365-2435.1999.00381.xCrossRefGoogle Scholar
  7. Cornelissen JHC, Lavorel S, Garnier E, et al. (2003) A hand book of protocols for standardized and easy measurement of plant functional traits worldwide. Australian Journal of Botany 51(4): 335–380. DOI: 10.1071/BT02124CrossRefGoogle Scholar
  8. Craig H (1957) Isotopic standards for carbon and oxygen and correction factors for mass-spectrometric analysis of carbon dioxide. Geochim Cosmochim Acta 12: 133–149. DOI: 10.1016/0016-7037(57)90024-8CrossRefGoogle Scholar
  9. Cunningham SA, Summerhayes B, Westoby M (1999) Evolutionary divergences in leaf structure and chemistry, comparing rainfall and soil nutrient gradients. Ecological Monographs 69(4): 569–588. DOI: 10.1890/0012-9615CrossRefGoogle Scholar
  10. Dias M, Pinto CG, Correia CM, et al. (2013) Photosynthetic parameters of Ulmus minor plantlets affected by irradiance during acclimatization. Biologia Plantarum 57(1): 33–40. DOI: 10.1007/s10535-012-0234-8CrossRefGoogle Scholar
  11. Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78(1): 9–19. DOI: 10.1007/BF00377192CrossRefGoogle Scholar
  12. Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 40: 503–537. DOI: 10.1146/annurev.pp.40.060189.002443CrossRefGoogle Scholar
  13. Farquhar GD, Buckley TN, Miller JM (2002) Optimal stomatal control in relation to leaf area and nitrogen content. Silva Fennica 36(3): 625–637. DOI: 10.14214/sf.530CrossRefGoogle Scholar
  14. Feng Y, Wen ZB, Gulnur S, et al. (2014) Study of the relationship between compositions of shrub plant of stablecarbon-isotope and environmental factors in Xinjiang Representatives of Chenopodiaceae. Contemporary Problems of Ecology 7(3): 301–307. DOI: 10.1134/S1995425514030056CrossRefGoogle Scholar
  15. Fonseca CR, Overton JM, Collins B, et al. (2000) Shifts in trait combinations along rainfall and phosphorus gradients. Journal of Ecology 88(6): 964–977. DOI: 10.1046/j.1365-2745.2000.00506.xCrossRefGoogle Scholar
  16. Friend AD, Woodward FI (1990) Evolutionary and ecophysiological responses of mountain plants to the growing season environment. Advances in Ecological Research 20: 59–124. DOI: 10.1016/S0065-2504(08)60053-7CrossRefGoogle Scholar
  17. Hao S, Liu P, Zhang YT, et al. (2007) Research of microclimatic characters of Tianshan Mountain spruce forest in the middle location of Tianshan Mountain. Journal of Xinjiang Agricultural University 30(1): 48–52. DOI: 10.3969/j.issn.1007-8614.2007.01.012 (in Chinese)Google Scholar
  18. Hultine KR, Marshall JD (2000) Altitude trends in conifer leaf morphology and stable carbon isotope composition. Oecologia 123(1): 32–40. DOI: 10.1007/s004420050986CrossRefGoogle Scholar
  19. Kao WY, Chang KW (2001) Altitudinal trends in photosynthetic rate and leaf characteristics of Miscanthus populations from central Taiwan. Australian Journal of Botany 49: 509–514. DOI: 10.1071/BT00028CrossRefGoogle Scholar
  20. Kong GQ, Luo TX, Liu XS, et al. (2012) Annual ring widths are good predictors of changes in net primary productivity of alpine Rhododendron shrubs in the Sergyemla Mountains, southeast Tibet. Plant Ecology 213: 1843–1855. DOI: 10.1007/s11258-012-0140-3CrossRefGoogle Scholar
  21. Knoll M, Achleitner D, Redl H (2006) Response of Zweigelt Grapevine to Foliar Application of Potassium Fertilizer: Effects on Gas Exchange, Leaf Potassium Content, and Incidence of Traubenwelke. Journal of Plant Nutrition 29(10): 1805–1817. DOI: 10.1080/01904160600899303CrossRefGoogle Scholar
  22. Korner C, Cochrane P (1985) Stomatal responses and water relations of Eucalyptus pauciflora in summer along an elevational gradient. Oecologia 66(3): 443–455. DOI: 10.1007/BF00378313CrossRefGoogle Scholar
  23. Korner C, Diemer M (1987) In situ photosynthetic responses to light, temperature, and carbon dioxide in herbaceous plants from low and high altitude. Functional Ecology 1(3): 179–194.CrossRefGoogle Scholar
  24. Korner C, Farquhar GD, Roksandic Z (1988) A global survey of carbon isotope discrimination in plants from high altitude. Oecologia 74(4): 623–632. DOI: 10.1007/BF00380063CrossRefGoogle Scholar
  25. Korner C (1989) The nutritional status of plants from high altitudes. Oecologia 81(3): 379–391. DOI: 10.1007/BF00377088CrossRefGoogle Scholar
  26. Korner C, Neumayer M, Palaez MRS, et al. (1989) Functional morphology of mountain plants. Flora 182: 353–383. DOI: can not findGoogle Scholar
  27. Korner C (1998) A re-assessment of high elevation treeline positions and their explanation. Oecologia 115: 445–459. DOI: 10.1007/s004420050540CrossRefGoogle Scholar
  28. Li CY, Liu XL, Berninger F (2004) Picea seedlings show apparent acclimation to drought with increasing altitude in the eastern Himalaya. Trees 18(3): 277–283. DOI: 10.1007/s00468-003-0304-9CrossRefGoogle Scholar
  29. Li, CY, Zhang, XJ, Liu XL, et al. (2006) Leaf morphological and physiological responses of Quercus aquifolioides along an altitudinal gradient. Silva Fennica 40(1): 5–13. DOI: 10.14214/sf.348CrossRefGoogle Scholar
  30. Li FL, Bao WK, Liu JH (2005) Leaf characteristics and their relationship of Cotinus coggygria in arid river valley located in the upper reaches of Minjiang River with environmental factors depending on its altitude gradients. Acta Botanica Boreali-occidentalia Sinica 25(11): 2277–2284. DOI: 10.3321/j.issn:1000-4025.2005.11.024 (in Chinese)Google Scholar
  31. Li JZ, Wang GA, Liu XZ, et al. (2009) Variations in carbon isotope ratios of C3 plants and distribution of C4 plants along an altitudinal transect on the eastern slope of Mount Gongga. Science in China Series D: Earth Sciences 52(11): 1714–1723. DOI: 10.1007/s11430-009-0170-4CrossRefGoogle Scholar
  32. Li XB, Chen JF, Zhang PZ, et al. (1999) The characteristics of carbon isotope composition of modern plants over Qinghai-Tibet plateau (NE) and its climatic information. Acta Sedi Mentol Sin 17(2): 325–329. DOI: 10.3969Zj.issn.1000-0550.1999.02.027 (in Chinese)Google Scholar
  33. Li XB, Bai ZQ, Guo ZJ, et al. (2001) Study on photosynthesis of Tianshan spruce and other main tree species. Xinjiang Agricultural Sciences 38(2): 62–65. DOI: 10.3969/j.issn.1001-4330.2001.02.004 (in Chinese)Google Scholar
  34. Li Y, Zhao HX, Duan BL, et al. (2011) Adaptability to elevated temperature and nitrogen addition is greater in a highelevation population than in a low-elevation population of Hippophae rhamnoides. Trees 25(6): 1073–1082. DOI: 10.1007/s00468-011-0582-6CrossRefGoogle Scholar
  35. Liu BH, Cheng L, Liang D, et al. (2012) Growth, gas exchange, water-use efficiency, and carbon isotope composition of ‘Gale Gala’ apple trees grafted onto 9 wild Chinese rootstocks in response to drought stress. Photosynthetica 50(3): 401–410. DOI: 10.1007/s11099-012-0048-0CrossRefGoogle Scholar
  36. Liu XH, Zhao LJ, Gasaw M, et al. (2007) Foliar δ13C and δ15N values of C3 plants in the Ethiopia Rift Valley and their environmental controls. Chinese Science Bulletin 52(9): 1265–1273. DOI: 10.1007/s11434-007-0165-5CrossRefGoogle Scholar
  37. Luo JX, Zang RG, Li CY (2006) Physiological and morphological variations of Picea asperata populations originating from different altitudes in the mountains of southwest China. Forest Ecology and Management 221(1): 285–290. DOI: 10.1016/j.foreco.2005.10.004CrossRefGoogle Scholar
  38. Magnani F, Borghetti M (1995) Interpretation of seasonal changes of xylem embolism and plant hydraulic resistance in Fagus sylvatica. Plant Cell and Environment 18(6): 689–696. DOI: 10.1111/j.1365-3040.1995.tb00570.xCrossRefGoogle Scholar
  39. Meinzer FC, Rundel PW, Goldstein G, et al. (1992) Carbon isotope composition in relation to leaf gas exchange and environmental conditions in Hawaiian Metrosideros polymorpha populations. Oecologia 91(3): 305–311. DOI: 10.1007/BF00317617CrossRefGoogle Scholar
  40. Morecroft MD, Woodward FI (1990) Experimental investigations on the environmental determination of δ 13C at different altitudes. Journal of Experimental Botany 41(10): 1303–1308. DOI: 10.1093/jxb/41.10.1303CrossRefGoogle Scholar
  41. Morecroft MD, Woodward FI, Marrs RH (1992) Attitudinal trends in leaf nutrient contents, leaf size and δ 13C of Alchemilla alpina. Functional Ecology 6(6): 730–740. DOI: 10.2307/2389970CrossRefGoogle Scholar
  42. Morecroft MD, Woodward FI (1996) Experiments on the causes of altitudinal differences in the leaf nutrient contents, size and δ 13C of Alchemilla alpina. New Phytologist 134(3): 471–479. DOI: 10.1111/j.1469-8137.1996.tb04364.xCrossRefGoogle Scholar
  43. Paridari IC, Jalali SG, Bruschi ASMZP (2013) Leaf macro- and micro-morphological altitudinal variability of Carpinus betulus in the Hyrcanian forest (Iran). Journal of Forestry Research 24(2): 301–307. DOI: 10.1007/s11676-013-0353-xCrossRefGoogle Scholar
  44. Piao HC, Zhu JM, Zhu SF, et al. (2004) Altitudinal variations of nutrient concentrations and carbon isotope compositions in a C3 plant and the effects of nutrient interactions on carbon isotope discrimination in limestone areas of southwest China. Advance in the earth Sciences 19 (Supplement): 412-418.Google Scholar
  45. Pu ZC, Zhang SQ, Li JL, et al. (2008) Change characteristics of reference crop evapotranspiration in Urumqi River basin. Desert and Oasis Meteorology 2(1): 41–45. DOI: 10.3969/j.issn.1002-0799.2008.01.011 (in Chinese)Google Scholar
  46. Qiang WY, Wang XL, Chen T, et al. (2003) Variations of stomatal density and carbon isotope values of Picea crassifolia at different altitudes in the Qilian Mountains. Trees 17(3): 258–262. DOI: 10.1007/s00468-002-0235-xGoogle Scholar
  47. Qi J, Ma KM, Zhang YX (2007) The altitudinal variation of leaf traits of Quercus liaotungensis and associated environmental explanations. Acta Ecologica Sinica 27(3): 0930–0937. DOI: 10.3321/j.issn:1000-0933.2007.03.013 (in Chinese)Google Scholar
  48. Ran F, Zhang XL, Zhang YB, et al. (2013) Altitudinal variation in growth, photosynthetic capacity and water use efficiency of Abies faxoniana Rehd. et Wils. seedlings as revealed by reciprocal transplantations. Trees 27(5): 1405–1416. DOI: 10.1007/s00468-013-0888-7CrossRefGoogle Scholar
  49. Robert JP (2002) The chequered history of the development and use of simultaneous equations for the accurate determination of chlorophylls a and b. Photosynthesis Research 73(1): 149–156. DOI: 10.1023/A:1020470224740Google Scholar
  50. Ridolfi M, Garrec JP (2000) Consequences of an excess Al and a deficiency in Ca and Mg for stomatal functioning and net carbon assimilation of beech leaves. Annals of Forest Science 57(3): 209–218. DOI: 10.1051/forest:2000112CrossRefGoogle Scholar
  51. Schroeder JI, Hagiwara S (1989) Cytosolic calcium regulates ion channels in the plasma membrane of Vicia faba guard cells. Nature 338(6214): 427–430. DOI: 10.1038/338427a0CrossRefGoogle Scholar
  52. Song MH, Duan DY, Chen H, et al. (2008) Leaf δ13C reflects ecosystem patterns and responses of alpine plants to the environments on the Tibetan Plateau. Ecography 31(4): 499–508. DOI: 10.1111/j.0906-7590.2008.05331.xCrossRefGoogle Scholar
  53. Sparks JP, Ehleringer JR (1997) Leaf carbon isotope discrimination and nitrogen content of riparian trees along an elevational gradient. Oecologia 109(3): 362–367. DOI: 10.1007/s004420050094CrossRefGoogle Scholar
  54. Su HX, Sang WG, Wang YX, et al. (2007) Simulating Picea schrenkiana forest productivity under climatic changes and atmospheric CO2 increase in Tianshan Mountains, Xinjiang Autonomous Region, China. For Ecol Manage 246: 273–284. DOI: 10.1016/j.foreco.2007.04.010CrossRefGoogle Scholar
  55. Sun X, Rao LH, Zhang YS, et al. (1989) Effect of Potassium Fertilizer Application on Physiological Parameters and Yield of Cotton grown on a Potassium deficient. Soil Journal of Plant Nutrition and Soil Science 152(3): 269–272. DOI: 10.1002/jpln.19891520301Google Scholar
  56. Tsialtas JT, Tokatlidis IS, Tsikrikoni C, et al. (2008) Leaf carbon isotope discrimination, ash content and K relationships with seedcotton yield and lint quality in lines of Gossypium hirsutum L. Field Crops Research 107(1): 70–77. DOI: 10.1016/j.fcr.2007.12.017CrossRefGoogle Scholar
  57. Van de Water PK, Leavitt SW, Betancourt JL (2002) Leaf δ 13C variability with elevation, slope aspect, and precipitation in the southwest United States. Oecologia 132(3): 332–343. DOI: 10.1007/s00442-002-0973-xCrossRefGoogle Scholar
  58. Vitousek PM, Field CB, Matson PA (1990) Variation in foliar δ 13C in Hawaiian Metrosideros polymorpha: a case of internal resistance? Oecologia 84(3): 362–370. DOI: 10.1007/BF00329760CrossRefGoogle Scholar
  59. Wang T, Liang Y, Ren HB, et al. (2004) Age structure of Picea schrenkiana forest along an altitudinal gradient in the central Tianshan Mountains, northwestern China. Forest Ecology and Management 196(2): 267–274. DOI: 10.1016/j.foreco.2004.02.063CrossRefGoogle Scholar
  60. Wang XF, Li RY, Li XZ, et al. (2014) Variations in leaf characteristics of three species of angiosperms with changing of altitude in Qilian Mountains and their inland high-altitude pattern. Science China Earth Sciences 57(4): 662–670. DOI: 10.1007/s11430-013-4766-3CrossRefGoogle Scholar
  61. Wang GA, Han JM, Faiiac A, et al. (2008) Experimental measurements of leaf carbon isotope discrimination and gas exchange in the progenies of Plantago depressa and Setaria viridis collected from a wide altitudinal range. Physiologia Plantarum 134(1): 64–73. DOI: 10.1111/j.1399-3054.2008.01102.xCrossRefGoogle Scholar
  62. Wilson J, Thompson K, Hodgson JG (1999) Specific leaf area and leaf dry matter content as alternative predictors of plants trategies. New Phytologist 143(1): 155–162. DOI: 10.1046/j.1469-8137.1999.00427.xCrossRefGoogle Scholar
  63. Witkowski ETF, Lamont BB (1991) Leaf specific mass confounds leaf density and thickness. Oecologia 88(4): 486–493. DOI: 10.1007/BF00317710CrossRefGoogle Scholar
  64. Woodward FI, Bazzaz FA (1988) The response of stomatal density to CO2 partial pressure. Journal of Experimental Botany 39: 1771–1781. DOI: 10.1093/jxb/39.12.1771CrossRefGoogle Scholar
  65. Xie SP, Sun BN, Yan DF, et al. (2009) Altitudinal variation in Ginkgo leaf characters: Clues to paleoelevation reconstruction. Science in China Series D-Earth Sciences 52(12): 2040–2046. DOI: 10.1007/s11430-009-0157-1CrossRefGoogle Scholar
  66. Yan CF, Han SJ, Zhou YM, et al. (2013) Needle δ13C and mobile carbohydrates in Pinus koraiensis in relation to decreased temperature and increased moisture along an elevational gradient in NE China. Trees 27(2): 389–399. DOI: 10.1007/s00468-012-0784-6CrossRefGoogle Scholar
  67. Yu DP, Wang QW, Liu JQ, et al. (2014) Formation mechanisms of the alpine Erman’s birch (Betula ermanii) treeline on Changbai Mountain in Northeast China. Trees 28(3): 935–947. DOI: 10.1007/s00468-014-1008-zCrossRefGoogle Scholar
  68. Zhao CM, Chen LT, Ma F, et al. (2008) Altitudinal differences in the leaf fitness of juvenile and mature alpine spruce trees (Picea crassifolia). Tree Physiology 28(1): 133–141. DOI: 10.1093/treephys/28.1.133CrossRefGoogle Scholar
  69. Zhang YS, Tang GC (1989) Picea schrenkiana forest. In: Editorial Committee of Xinjiang Forest (Eds.), Xinjiang Forest. Chinese Forestry Press, Beijing, China. (in Chinese)Google Scholar
  70. Zhang YF, Chen T, An LZ, et al. (2007) The variations of stablecarbon isotope ratios in Qilian juniper in northwestern China. Environmental Geology 52(1): 131–136. DOI: 10.1007/s00254-006-0466-zCrossRefGoogle Scholar
  71. Zhang ZL (1990) Guidance of plant physiology experiments. Higher Education Press, Beijing, China. (in Chinese)Google Scholar
  72. Zhou YC, Fan JW, Zhong HP, et al. (2013) Relationships between altitudinal gradient and plant carbon isotope composition of grassland communities on the Qinghai-Tibet Plateau, China. Science China: Earth Sciences 56(2): 311–320. DOI: 10.1007/s11430-012-4498-9CrossRefGoogle Scholar
  73. Zhu Y, Siegwolf RTW, Durka W, et al. (2010) Phylogenetically balanced evidence for structural and carbon isotope responses in plants along elevational gradients. Oecologia 162(4): 853–863. DOI: 10.1007/s00442-009-1515-6CrossRefGoogle Scholar

Copyright information

© Science Press, Institute of Mountain Hazards and Environment, CAS and Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.State Key Laboratory Breeding Base of Desertification and Aeolian Sand Disaster CombatingGansu Desert Control Research InstituteLanzhouChina
  2. 2.Key Laboratory of Ecohydrology of Inland River Basin, Cold and Arid Regions Environmental and Engineering Research InstituteChinese Academy of SciencesLanzhouChina
  3. 3.Key Laboratory of Western China’s Environmental Systems (Ministry of Education)Lanzhou UniversityLanzhouChina
  4. 4.Lanzhou Institute of SeismologyChina Earthquake AdministrationLanzhouChina

Personalised recommendations