Journal of Mountain Science

, Volume 13, Issue 6, pp 1066–1077 | Cite as

Altitudinal trends in δ13C value, stomatal density and nitrogen content of Pinus tabuliformis needles on the southern slope of the middle Qinling Mountains, China

  • Xian-zhao LiuEmail author
  • Chang-chun Gao
  • Qing Su
  • Yong Zhang
  • Yan Song


In this study, a coniferous tree species (Pinus tabuliformis Carr.) was investigated at a moderate-altitude mountainous terrain on the southern slope of the middle Qinling Mountains (QLM) to detect the trends in carbon isotope ratio (δ13C), leaf nitrogen content (LNC) and stomatal density (SD) with altitude variation in north-subtropical humid mountain climate zone of China. The results showed that LNC and SD both significantly increased linearly along the altitudinal gradient ranging from 1000 to 2200 m, whereas leaf δ13C exhibited a significantly negative correlation with the altitude. Such a correlation pattern differs obviously from that obtained in offshore low-altitude humid environment or inland high-altitude semi-arid environment, suggesting that the pattern of increasing δ13C with the altitude cannot be generalized. The negative correlation between δ13C and altitude might be attributed mainly to the strengthening of carbon isotope fractionation in plants caused by increasing precipitation with altitude. Furthermore, there was a remarkable negative correlation between leaf δ13C and LNC. One possible reason was that increasing precipitation that operates to increase isotopic discrimination with altitude overtook the LNC in determining the sign of leaf δ13C. The significant negative correlation between leaf δ13C and SD over altitudes was also found in the present study, indicating that increases in SD with altitude would reduce, rather than enhance plant δ13C values.


Carbon isotope ratio Nitrogen content Stomatal density Altitudinal variation Qinling Mountains 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Andrés V, Tuanmu MN, Xu WH, et al. (2012) Relationship between floristic similarity and vegetated land surface phenology: Implications for the synoptic monitoring of species diversity at broad geographic regions. Remote Sensing of Environment 121: 488–496. DOI:10.1016/j.rse.2012.02.013CrossRefGoogle Scholar
  2. Beerling DJ (1999) Stomatal density and index: Theory and application. Burlington House, London, UK. pp 251–254.Google Scholar
  3. Beerling DJ, Kelly CK (1996) Evolutionary comparative analysis of the relationship between leaf structure and function. New Phytologist 134: 35–51. DOI: 10.1111/j.1469-8137.1996.tb01144.xCrossRefGoogle Scholar
  4. Beerling DJ, Osborne CP, Chaloner WG (2001) Evolution of leaf-form in land plants linked to atmospheric CO2 decline in the late Palaeozoic era. Nature 410: 352–354. DOI: 10.1038/35066546CrossRefGoogle Scholar
  5. Beerling DJ, Chaloner WG (2011) The impact of atmospheric CO2 and temperature change on stomatal density: Observations from Quercus roburlammas leaves. Annals Botany 71: 231–235. DOI: 10.1006/anbo.1993.1029CrossRefGoogle Scholar
  6. Bramley-Alves J, Wanek W, French K, et al. (2015) Moss d13C: an accurate proxy for past water environments in polar regions. Global Change Biology 21: 2454–2464. DOI: 10.1111/gcb.12848CrossRefGoogle Scholar
  7. Carrer M, Nola P, Eduard JL, et al. (2007) Regional variability of climate-growth relationships in Pinus cembra high elevation forests in the Alps. Journal of Ecology 95: 1072–1083. DOI: 10.1111/j.1365-2745.2007.01281.xCrossRefGoogle Scholar
  8. Chen LQ, Cheng SL, Chaloner WG, et al. (2001) Assessing the potential for the stomatal characters of extent and fossil Ginkgo leaves to signal atmosphere CO2 change. American Journal of Botany 88: 1309–1315. DOI: 10.2307/3558342CrossRefGoogle Scholar
  9. Chen JW, Yang ZQ, Zhou P, et al. (2013) Biomass accumulation and partitioning, photosynthesis, and photosynthetic induction in field-grown maize (Zea mays L.) under low and high nitrogen conditions. ActaPhysiologiaePlantarum 35: 95–105. DOI: 10.1007/s11738-012-1051-6Google Scholar
  10. Chinese Soil Society (1999) Chemical Analysis of Soil. Chinese Agricultural Science Press, Beijing, China. pp 32–40. (In Chinese)Google Scholar
  11. Cordell S, Goldstein G, Meinzer FC, et al. (1999) Allocation of nitrogen and carbon in leaves of Metrosideros polymorpha regulates carboxylation capacity and δ13C along an altitudinal gradient. Functional Ecology 13: 811-818. DOI: 10.1046/j. 1365-2435.1999.00381.xGoogle Scholar
  12. Dang HS, Zhang YJ, Zhang KR, et al. (2010) Age structure and regeneration of subalpine fir (Abies fargesii) forests across an altitudinal range in the Qinling Mountains, China. Forest Ecology and Management 259: 547–554. DOI: 10.1016/j.foreco.2009.11.011CrossRefGoogle Scholar
  13. Diefendorf AF, Mueller KE, Wing SL, et al. (2010) Global patterns in leaf 13C discrimination and implications for studies of past and future climate. PNAS 107(13): 5738–5743. DOI: 10.1073/pnas.0910513107CrossRefGoogle Scholar
  14. Dong LM, Liu SM, Xin JH (1995) Variations of the climatic elements with elevation at Huoditang forest farm in Qinling Mountain range. Bulletin of soil and water conservation 15: 16–19. (In Chinese)Google Scholar
  15. 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: 301–307. DOI: 10.1134/S1995425514030056CrossRefGoogle Scholar
  16. Guan LL, Wen DZ (2011) More nitrogen partition in structural proteins and decreased photosynthetic nitrogen-use efficiency of Pinus massoniana under in situ polluted stress. Journal of Plant Research 124(6): 663–673. DOI: 10.1007/s10265-011-0405-2CrossRefGoogle Scholar
  17. Helliker B, Richter S (2008) Subtropical to boreal convergence of tree-leaf temperatures. Nature 454: 511–514. DOI: 10.1038/nature07031CrossRefGoogle Scholar
  18. Hietz P, Wanek W, Popp M (1999) Stable isotopic composition of carbon and nitrogen and nitrogen content in vascular epiphytes along an altitudinal transect. Plant, Cell and Environment 22: 1435–1443. DOI: 10.1046/j.1365-3040.1999.00502.xCrossRefGoogle Scholar
  19. Hikosaka K, Nagamatsu D, Ishii HS, et al. (2002) Photosynthesis-nitrogen relationships in species at different altitudes on Mount Kinabalu, Malaysia. Ecological Research 17: 305–313. DOI: 10.1046/j.1440-1703.2002.00490.xCrossRefGoogle Scholar
  20. Hultine KR, Marshall JD (2000) Altitude trends in conifer leaf morphology and stable carbon isotope composition. Oecologia 123: 32–40. DOI: 10.1007/s004420050986CrossRefGoogle Scholar
  21. Kogami H, Hanba YT, Kibe T, et al. (2001) CO2 transfer conductance, leaf structure and carbon isotope composition of Polygonum cuspidatum leaves from low and high altitudes. Plant, cell and environment 24: 529–538. DOI: 10.1046/j.1365-3040.2001.00696.xCrossRefGoogle Scholar
  22. Kouwenberg CLR, Kürschner WM, Kürschner WM (2007) Stomatal frequency change over altitudinal gradients: prospects for paleoaltimetry. Reviews in Mineralogy & Geochemistry 66: 215–241. DOI: 10.2138/rmg.2007.66.9CrossRefGoogle Scholar
  23. Lars K, Thomas G, Christop H (2006) Altitudinal change in soil and foliar nutrient concentrations and in microclimate across the tree line on the subtropical island mountain Mt. Teide (Canary Islands). Flora 3: 202–214. DOI: 10.1016/j.flora.2005.07.003Google Scholar
  24. Li C, Zhang X, Liu X, et al. (2006) Leaf morphological and physiological responses of Quercus aquifolioides along an altitudinal gradient. Silva Fennica 40: 5–13. DOI: 10.14214/sf.348CrossRefGoogle Scholar
  25. Li YB, Chen T, Zhang YF, et al. (2007) The relation of seasonal pattern in stable carbon compositions to meteorological variables in the leaves of Sabina przewalskii Kom. and Sabina chinensis (Lin.) Ant. Environmental Geology 51: 1279–1284. DOI: 10.1007/s00254-006-0421-zCrossRefGoogle Scholar
  26. 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: 1073–1082. DOI: 10.1007/s00468-011-0582-6CrossRefGoogle Scholar
  27. Li J, Wang G, Liu X, et al. (2009) Variations in carbon isotope ratios of C3plants and distribution of C4 plants along an altitudinal transect on the eastern slope of Mount Gongga. Science in China D: Earth Sciences 52: 1714–1723. DOI: 10.1007/s11430-009-0170-4CrossRefGoogle Scholar
  28. Liu XZ, Su Q, Li CK, et al. (2014) Responses of carbon isotope ratios of C3 herbs to humidity index in northern China. Turkish Journal of Earth Sciences 23: 100–111. DOI: 10.3906/yer-1305-2CrossRefGoogle Scholar
  29. Liu XH, Zhao LJ, Menassie G, et al. (2007) Foliar δ13C and d15N values of C3 plants in the Ethiopia Rift Valley and their environmental controls. Chinese Science Bulletin 9: 1265–1273. DOI: 10.1007/s11434-007-0165-5CrossRefGoogle Scholar
  30. Liu Y, Linderholm HW, Song HM, et al. (2008) Temperature variations recorded in Pinus tabulaeformis tree rings from the southern and northern slopes of the central Qinling Mountains, central China. Boreas 38: 285–291. DOI: 10.1111/j.1502-3885.2008.00065.xCrossRefGoogle Scholar
  31. Lockheart MJ, Poole I, Van Bergen PF, et al. (1998) Leaf carbon isotope composition and stomatal characters: important consideration for palaeoclimate reconstructions. Organic Geochemistry 29: 1003–1008. DOI: 10.1016/S0146-6380(98) 00168-5CrossRefGoogle Scholar
  32. Lu YD, Sun JZ, Li TL, et al. (2005) Application of carbon isotope in Chinese loess to semi-quantitative estimation of palaeotemperature. Marine Geolog y & Quaternary Geology 3: 139–143. (In Chinese).Google Scholar
  33. Luo JX, Zang RG, Li CY. (2006) Physiological and morphological variations of Picea asperata populations originating from different altitudes in the mountains of southwestern China. Forest Ecology and Management 221: 285–290. DOI: 10.1016/j.foreco.2005.10.004CrossRefGoogle Scholar
  34. McCarroll D, Pawellek F (2001) Stable carbon isotope ratios of Pinussylvestris from northern Finland and the potential for extraction a climate signal from long Fennoscandian chronologies. Holocene 11: 517–526. DOI: 10.1191/09596 8301680223477CrossRefGoogle Scholar
  35. Morecroft MD, Woodward FI (1996) Experiments on the causes of altitudinal differences in the leaf nutrient contents, size and δ13C of Alchemilla alpine. New Phytologist 134: 471–479. DOI: 10.1111/j.1469-8137.1996.tb04364.xCrossRefGoogle Scholar
  36. Nogues S, Allen DJ, Morison JI, et al. (1999) Characterization of stomatal closure caused by ultraviolet-B radiation. Plant Physiology 121: 489–496. DOI: 10.1104/pp.121.2.489CrossRefGoogle Scholar
  37. Oindrila D, Wang Y, Joseph DH, et al. (2013) Reconstruction of paleostorms and paleoenvironment using geochemical proxies archived in the sediments of two coastal lakes in northwest Florida. Quaternary Science Reviews 68: 142–153. DOI: 10.1016/j.quascirev.2013.02.014CrossRefGoogle Scholar
  38. Poorter H, Evans JR (1998) Photosynthetic nitrogen-use efficiency of species that differ inherently in specific leaf area. Oecologia 116: 26–37. DOI: 10.1007/s004420050560CrossRefGoogle Scholar
  39. Prasolova NV, Xu ZH, Farquhar GD, et al. (2000) Variation in branchlet δ13C in relation to branchlet nitrogen concentration and growth in 8-year-old hoop pine families (Araucaria cunninghamii) in subtropical Australia. Tree Physiology 20: 1049–1055. DOI: 10.1093/treephys/20.15.1049CrossRefGoogle Scholar
  40. 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: 258–262. DOI: 10.1007/s00468-002-0235-xGoogle Scholar
  41. Ran F, Zhang X, Zhang Y, 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: 1405–1416. DOI: 10.1007/s00468-013-0888-7Google Scholar
  42. Reich PB, Kloeppel BD, Ellsworth DS (1995) Different photosynthesis-nitrogen relations in deciduous hardwood and evergreen coniferous tree species. Oecologia 104: 24–30.DOI: 10.1007/BF00365558CrossRefGoogle Scholar
  43. 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: 209–218. DOI: 10.1051/forest:2000112CrossRefGoogle Scholar
  44. Royer DL (2001) Stomatal density and stomatal index as indicators of paleoatmospheric CO2 concentration. Review Palaeobotany and Palynology 114: 1–28. DOI: 10.1016/S0034-6667(00)00074-9CrossRefGoogle Scholar
  45. Saurer M, Cherubini P, Reynolds-Henne CE, et al. (2008) An investigation of the common signal in tree-ring stable isotope chronologies at temperate sites. Journal of Geophysical Research Atmospheres 113 (G4): 681–687. DOI: 10.1029/2008JG000689CrossRefGoogle Scholar
  46. Schulze ED, Schulze REW, Trimborn P, et al. (1996) Diversity, metabolic types and carbon isotope ratios in the grass flora of Namibia in relation to growth form, precipitation and habitat conditions. Oecologia 106: 352–369. DOI: 10.1007/BF00334563CrossRefGoogle Scholar
  47. Shi W, Wang G, Han W (2012) Altitudinal variation in leaf nitrogen concentration on the eastern slope of Mount Gongga on the Tibetan Plateau, China. PLoS ONE 7(9): e44628. DOI:10.1371/journal.pone.0044628CrossRefGoogle Scholar
  48. Shi ZM, Liu SR, Liu XL, et al. (2006). Altitudinal variation in photosynthetic capacity, diffusional conductance andd13Cof butterfly bush (Buddleja davidii) plants growing at high elevations. Physiologia Plantarum 128: 722–731. DOI: 10.1111/j.1399-3054.2006.00805.xCrossRefGoogle Scholar
  49. Smith WK, Hughes NM (2009) Progress in coupling plant formand photosynthetic function. Castanea 74: 1–26. DOI: 10.2179/08-009R5.1CrossRefGoogle Scholar
  50. Song X, Barbour MM, Saurer M, et al. (2011). Examining the large-scale convergence of photosynthesis-weighted tree-leaf temperatures through stable oxygen isotope analysis of multiple datasets. New Phytologist 192: 912–924. DOI: 10.1111/j.1469-8137.2011.03851.xCrossRefGoogle Scholar
  51. Sparks JP, Ehleringer JR (1997) Leaf carbon isotope discrimination and nitrogen content for riparian trees along elevational transects. Oceologia 109: 362–367. DOI: 10.1007/s004420050094CrossRefGoogle Scholar
  52. Sun BN, Wu JY, Liu YS, et al. (2011) Reconstructing neogene vegetation and climates to infer tectonic uplift in western Yunnan China. Paleogeography, Paleoclimatology, Paleoecology 304: 328–336. DOI: 10.1016/j.palaeo.2010.09.023CrossRefGoogle Scholar
  53. Tausz M, Peters J, Jimenez MS (1998) Element contents and stress-physiological characterization of Pinus canariensis needles in Mediterranean type field stands in Tenerife. Chemosphere 36: 1019–1023. DOI: 10.1016/S0045-6535(97)10165-5CrossRefGoogle Scholar
  54. Van de Water PK, Leavitt SW, Betancourt JL (2002) Leaf δ13C variability with elevation, slope aspect and precipitation in the southwest United States. Oecologia 132: 332–343. DOI: 10.1007/s00442-002-0973-xCrossRefGoogle Scholar
  55. Valery JT, Zewdu E, Albert C, et al. (2008) Reconstructing palaeoenvironment from δ13C and d15N values of soil organic matter: A calibration from arid and wetter elevation transects in Ethiopia. Geoderma 147: 197–210. DOI: 35400018444324.0130CrossRefGoogle Scholar
  56. van Hoof TB, Kürschner WM, Wagner F, et al. (2006) Stomatal index response of Quercus robur and Quercus petraea to the anthropogenic atmospheric CO2 increase. Plant Ecology 183: 237–243. DOI: 10.1007/s11258-005-9021-3CrossRefGoogle Scholar
  57. Wang GA, Zhou LP, Liu M, et al. (2010) Altitudinal trends of leaf δ13C follow different patterns across a mountainous terrain in north China characterized by a temperate semihumid climate. Rapid Communications in Mass Spectrometry 24: 1557–1564. DOI: 10.1002/rcm.4543CrossRefGoogle Scholar
  58. Wang GA, Li JZ, Liu XZ, et al. (2013) Variations in carbon isotope ratios of plants across a temperature gradient along the 400 mm isoline of mean annual precipitation in north China and their relevance to paleovegetation reconstruction. Quaternary Science Reviews 63: 83–90. DOI: 10.1016/j.quascirev.2012.12.004CrossRefGoogle Scholar
  59. 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: 662–670. DOI: 10.1007/s11430-013-4766-3CrossRefGoogle Scholar
  60. Wittich B, Horna V, Homeier J, et al. (2012) Altitudinal change in the photosynthetic capacity of tropical trees: a case study from Ecuador and a pantropical literature analysis. Ecosystems 15: 958–973. DOI: 10.1007/s10021-012-9556-9CrossRefGoogle Scholar
  61. Wu H, Wang DX, Huang QP, et al. (2012). Influence of environmental factors on species diversity of Pine-oak mixed forest in the middle part of south Qingling Mountains. Journal of Sci-Tech University of Northwest Agriculture and Forestry (Natural science edition) 9: 41–50. DOI: 10.13207/j.cnki.jnwafu.2012.09.002Google Scholar
  62. Xie SP, Sun BN, Yan DF, et al. (2006) Leaf cuticular characters of Ginkgo and implications for paleo-atmospheric CO2 in the Jurassic. Progress in Natural Science 16: 258–263. DOI: 10.1080/10020070612330091CrossRefGoogle Scholar
  63. Xie SP, Sun BN, Yan DF, et al. (2009) Altitudinal variation in Ginkgo leaf characters: clues to paleoelevation reconstruction. Science China (Earth Sciences) 52: 2040–2046. DOI: 10.1007/s11430-009-0157-1CrossRefGoogle Scholar
  64. Xu ZZ, Zhou GS, Wang YH (2007) Combined effects of elevated CO2 and soil drought on carbon and nitrogen allocation of the desert shrub Caragana intermedia. Plant Soil 301: 87–97. DOI: 10.1007/s11104-007-9424-0CrossRefGoogle Scholar
  65. Yan C, Han S, Zhou Y, 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: 389–399. DOI: 10.1007/s00468-012-0784-6CrossRefGoogle Scholar
  66. Zhang HW, Ma JY, Sun W, et al. (2014) Variations in stable carbon isotope composition and leaf traits of Piceas chrenkiana var. tianschanica along an altitude gradient in Tianshan Mountains, northwest China. The Scientific World Journal 2014: 1–10. DOI: 10.1155/2014/243159Google Scholar
  67. Zhang P, Wang G, Zhang T, et al. (2010) Responses of foliar δ13C in Sabinaprzewalskii and Piceacrassifolia to altitude and its mechanism in the Qilian Mountains, China. Chinese Journal of Plant Ecology 34: 125–133. (In Chinese). DOI: 10.3773/j.issn.1005-264x.2010.02.003Google Scholar
  68. Zhao C, Chen L, Ma F, et al. (2008) Altitudinal differences in the leaf fitness of juvenile and mature alpine spruce trees (Piceacrassifolia). Tree Physiology 28: 133–141. DOI: 10.1093/treephys/28.1.133CrossRefGoogle Scholar
  69. Zhao LJ, Xiao HL, Liu XH (2006) Variations of foliar carbon isotope discrimination and nutrient concentrations in Artemisia ordosica and Caraganakorshinskii at the southeastern margin of China’s Tengger Desert. Environmental Geology 50: 285–294. DOI: 10.1007/s00254-006-0209-1CrossRefGoogle Scholar
  70. Zhou YC, Fan JW, Harris W, et al. (2013) Relationships between C3 plant foliar carbon isotope composition and element contents of grassland species at high altitudes on the Qinghai-Tibet Plateau, China. PLoS ONE 8: e60794. DOI: 10.1371/journal.pone.0060794CrossRefGoogle Scholar
  71. Zhou YC, Fan JW, Zhang WY, et al. (2011) Factors influencing altitudinal patterns of C3 plant foliar carbon isotope composition of grasslands on the Qinghai-Tibet Plateau, China. Alp Botany 121: 79–90. DOI: 10.1007/s00035-011-0093-5CrossRefGoogle Scholar
  72. 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: 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

  • Xian-zhao Liu
    • 1
    • 2
    Email author
  • Chang-chun Gao
    • 1
  • Qing Su
    • 3
  • Yong Zhang
    • 2
  • Yan Song
    • 2
  1. 1.College of Architecture and Urban PlanningHunan University of Science and TechnologyXiangtanChina
  2. 2.State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil ScienceChinese Academy of SciencesNanjingChina
  3. 3.College of Life ScienceHunan University of Science and TechnologyXiangtanChina

Personalised recommendations