Skip to main content
SpringerLink
Log in

Causes for the unimodal pattern of leaf carbon isotope composition in Abies faxoniana trees growing in a natural forest along an altitudinal gradient

  • Published:
Journal of Mountain Science Aims and scope Submit manuscript

Abstract

Leaf morphological and physiological traits of Abies faxoniana growing in a natural forest along an altitudinal gradient were measured with the aim to identify the central mechanism for the marked variation in foliar δ13C determined by an isotope ratio mass spectrometer. There is a unimodal pattern of plant functional traits in these temperate and semi-humid areas. Stomatal parameters, specific leaf area, and C/N ratio increased, whereas C, N and δ13C values decreased with increasing altitude below 3000 m a.s.l.. In contrast, they exhibited opposite trends above 3000 m a.s.l.. Our results demonstrated that high-altitude plants achieve higher water use efficiency (WUE) at the expense of decreasing nitrogen use efficiency (NUE), whereas plants at 3000 m can maintain a relatively higher NUE but a lower WUE. Such intra-specific differences in the trade-off between NUE and WUE may partially explain the altitudinal distribution of the plants in relation to moisture and nutrient availability. Our results clearly indicate that the functional relations between nutritional status and the structure of leaves are responsible for the altitudinal variations associated with δ13C. The pivotal role of specific leaf area in regulating plant adaptive responses provides a potential physiological mechanism for the observed growth advantage of populations occupying the medium altitude. These adaptive responses to altitudinal gradients showed that an altitude of approximately 3000 m a.s.l. is the optimum distribution zone for A. faxoniana, allowing the most vigorous growth and metabolism. These results improve our understanding of the various roles of environmental and biotic variables upon δ13C dynamics and provide useful information for subalpine coniferous forest management.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

C/N:

carbon/nitrogen ratio

δ13C:

carbon isotope composition

NUE:

nitrogen use efficiency

SD:

stomatal density

SI:

stomatal index

SL:

stomatal length

SLA:

specific leaf area

WUE:

water use efficiency

References

  • Bresson CC, Vitasse Y, Kremer A, et al. (2011) To what extent is altitudinal variation of functional traits driven by genetic adaptation in European oak and beech? Tree Physiology 31: 1164–1174. DOI: 10.1093/treephys/tpr084.

    Article  Google Scholar 

  • Chapin FS, Schulze ED, Mooney HA (1990) The ecology and economics of storage in plants. Annual Review of Ecology, Evolution, and Systematics 21: 423–447. DOI: 10.1146/annurev.ecolsys.21.1.423.

    Article  Google Scholar 

  • Chen S, Bai Y, Zhang L, et al. (2005) Comparing physiological responses of two dominant grass species to N addition in Xilin River Basin of China. Environmental and Experimental Botany 53: 65–75. DOI:10.1016/j.envexpbot.2004.03.002.

    Article  Google Scholar 

  • Escudero A, Mediavilla S (2003) Decline in photosynthetic nitrogen use efficiency with leaf age and nitrogen resorption as determinants of leaf life span. Journal of Ecology 91: 880–889. DOI: 10.1046/j.1365-2745.2003.00818.x.

    Article  Google Scholar 

  • 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.arplant.40.1.503

    Article  Google Scholar 

  • Feng Y, Li Y, Wang R, et al. (2011) A quicker return energy-use strategy by populations of a subtropical invader in the nonnative range: a potential mechanism for the evolution of increased competitive ability. Journal of Ecology 99: 1116–1123. DOI: 10.1111/j.1365-2745.2011.01843.x

    Article  Google Scholar 

  • Flanagan LB, Farquhar GD (2014) Variation in the carbon and oxygen isotope composition of plant biomass and its relationship to water-use efficiency at the leaf- and ecosystem-scales in a northern Great Plains grassland. Plant Cell and Environment 37: 425–438. DOI: 10.1111/pce.12165.

    Article  Google Scholar 

  • Grace JB (2006) Structural equation modeling and natural systems. Cambridge: Cambridge University Press.

    Book  Google Scholar 

  • Hubick KT, Farquhar GD, Shorter R (1986) Correlation between water-use efficiency and carbon isotope discrimination in diverse peanut (Arachis) germplasm. Australian Journal of Plant Physiology 13: 803–816. DOI: 10.1071/PP9860803.

    Article  Google Scholar 

  • Hultine KR, Marshall JD (2000) Altitude trends in conifer leaf morphology and stable carbon isotope composition. Oecologia 123: 32–40. DOI:10.1007/s004420050986.

    Article  Google Scholar 

  • Kim E, Donohue K (2013) Local adaptation and plasticity of Erysimum capitatum to altitude: its implications for responses to climate change. Journal of Ecology 101: 796–805. DOI:10.1111/1365-2745.12077.

    Article  Google Scholar 

  • Körner C (1989) The nutritional status of plants from high altitudes: a worldwide comparison. Oecologia 81: 379–391. DOI: 10.1007/BF00377088.

    Article  Google Scholar 

  • Körner C, Farquhar GD, Roksandic S (1988) A global survey of carbon isotope discrimination in plants from high altitude. Oecologia 74: 623–632. DOI: 10.1007/BF00380063.

    Article  Google Scholar 

  • Körner C, Farquhar GD, Wong SC (1991) Carbon isotope discrimination by follows latitudinal and altitudinal trends. Oecologia 88: 30–40. DOI: 10.1007/BF00328400.

    Article  Google Scholar 

  • Kurokawa H, Nakashizuka T (2008) Leaf herbivory and decomposability in a Malaysian tropical rain forest. Ecology 89: 2645–2656. DOI:10.1890/07-1352.1.

    Article  Google Scholar 

  • Lande R (2009) Adaptation to an extraordinary environment by evolution of phenotypic plasticity and genetic assimilation. Journal of Evolutionary Biology 22: 1435–1446. DOI: 10.1111/j.1420-9101.2009.01754.x.

    Article  Google Scholar 

  • Lei Y, Wang W, Feng Y, et al. (2012) Synergistic interactions of CO2 enrichment and nitrogen deposition promote growth and ecophysiological advantages of invading Eupitorium adenophorum in Southwest China. Planta 236: 1205–1213. DOI: 10.1007/s00425-012-1678-y.

    Article  Google Scholar 

  • Li C, Wu C, Duan B, et al. (2009) Age-related nutrient content and carbon isotope composition in the leaves and branches of Quercus aquifolioides along an altitudinal gradient. Trees-Structure and Function 23: 1109–1121. DOI: 10.1007/s00468-009-0354-8.

    Article  Google Scholar 

  • Li C, Xu G, Zang R, et al. (2007) Sex-related differences in leaf morphological and physiological responses in Hippophae rhamnoides along an altitudinal gradient. Tree Physiology 27: 399–406. DOI: 10.1093/treephys/27.3.399.

    Article  Google Scholar 

  • Lienin P, Kleyer M (2012) Plant trait responses to the environment and effects on ecosystem properties. Basic and Applied Ecology 13: 301–311. DOI:10.1016/j.baae.2012.05.002.

    Article  Google Scholar 

  • Li R, Luo T, Tang Y, et al. (2013) The altitudinal distribution center of a widespread cushion species is related to an optimum combination of temperature and precipitation in the central Tibetan Plateau. Journal of Arid Environments 88: 70–77. DOI:10.1016/j.jaridenv.2012.07.018.

    Article  Google Scholar 

  • Livingston NJ, Guy RD, Ethier GJ (1999) The effects of nitrogen stress on the stable carbon isotope composition, productivity and water use efficiency of white spruce (Picea glauca (Moench) Voss) seedlings. Plant Cell and Environment 22: 281–289. DOI: 10.1046/j.1365-3040.1999.00400.x.

    Article  Google Scholar 

  • Loomis RS (1997) On the utility of nitrogen in leaves. Proceedings of the National Academy of Sciences of United States of America 94: 13378–13379. DOI: 10.1073/pnas.94.25.13378.

    Article  Google Scholar 

  • Morecroft MD, Woodward FI (1996) Experiments on the causes of altitudinal differences in leaf nutrient contents, age and 13C of Alchemilla alpina. New Phytologist 134: 471–479. DOI: 10.1111/j.1469-8137.1996.tb04364.x.

    Article  Google Scholar 

  • Pan S, Liu C, Zhang W, et al. (2013) The scaling relationships between leaf mass and leaf area of vascular plant species change with altitude. PLoS ONE 8(10): e76872. DOI: 10.1371/journal.pone.0076872.

    Article  Google Scholar 

  • Peuke AD, Gessler A, Rennenberg H (2006) The effect of drought on C and N stable isotopes in different fractions of leaves, stems and roots of sensitive and tolerant beech ecotypes. Plant Cell and Environment 29: 823–835. DOI: 10.1111/j.1365-3040.2005.01452.x.

    Article  Google Scholar 

  • Poorter H, Niinemets U, Poorter L, et al. (2009) Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytologist 182: 565–588. DOI: 10.1111/j.1469-8137.2009.02830.x.

    Article  Google Scholar 

  • Prasolova NV, Xu ZH, Lundkvist K (2005) Genetic variation in foliar nutrient concentration in relation to foliar carbon isotope composition and tree growth with clones of the F-1 hybrid between slash pine and Caribbean pine. Forest Ecology and Management 210: 173–191. DOI: 10.1016/j.foreco.2005.02.029.

    Article  Google Scholar 

  • Qiang W, Wang X, Chen T, et al. (2003) Variation in stomatal density and carbon isotope values in Picea crassifolia at different altitudes in Qilian Mountains. Trees-Structure and Function 17: 258–262. DOI: 10.1007/s00468-002-0235-x.

    Google Scholar 

  • 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-Structure and Function 27: 1405–1416. DOI: 10.1007/s00468-013-0888-7.

    Article  Google Scholar 

  • 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.0044628.

    Article  Google Scholar 

  • Sparks JP, Ehleringer JR (1997) Leaf carbon isotope discrimination and nitrogen content for riparian trees along an elevational gradient. Oecologia 109: 362–367. DOI:10.1007/s004420050094.

    Article  Google Scholar 

  • Sultan SE (2000) Phenotypic plasticity for plant development, function, and life-history. Trends in Plants Science 5: 537–542. DOI: 10.1016/S1360-1385(00)01797-0.

    Article  Google Scholar 

  • Takashima T, Hikosaka K, Hirose T (2004) Photosynthesis or persistence: nitrogen allocation in leaves of evergreen and deciduous Quercus species. Plant Cell and Environment 27: 1047–1054. DOI: 10.1111/j.1365-3040.2004.01209.x.

    Article  Google Scholar 

  • Tanner EVJ, Vitousek PM, Cuevas E (1998) Experimental investigation of nutrient limitation of forest growth on wet tropical mountains. Ecology 79: 10–22. DOI: 10.2307/176860.

    Article  Google Scholar 

  • Vitousek PM, Field CB, Matson PA (1990) Variation in foliar δ13C in Hawaiian Metrosideros polymorpha: a case of internal resistance? Oecologia 84: 362–370. DOI: 10.1007/BF00329760.

    Article  Google Scholar 

  • Wang G, Feng X (2012) Response of plants’ water use efficiency to increasing atmospheric CO2 concentrations. Environmental Science and Technology 46: 8610–8620. DOI: 10.1021/es301323m.

    Article  Google Scholar 

  • Wang G, Zhou L, Liu M, et al. (2010) Altitudinal trends of leaf δ13C follow different patterns across a mountainous terrain in north China characterized by a temperate semi-humid climate. Rapid Communications in Mass Spectrometry 24: 1557–1564. DOI: 10.1002/rcm.4543.

    Article  Google Scholar 

  • Wang N, Xu S, Jia X, et al. (2013) Variations in foliar stable carbon isotopes among functional groups and along environmental gradients in China- a meta-analysis. Plant Biology 15: 144–151. DOI: 10.1111/j.1438-8677.2012.00605.x.

    Article  Google Scholar 

  • Zas R, Serrada R (2003) Foliar nutrient status and nutritional relationships of young Pinus radiata D. Don plantations in northwest Spain. Forest Ecology and Management 174: 167–176. DOI: 10.1016/S0378-1127(02)00027-0.

    Article  Google Scholar 

  • Zhang L, Luo TX, Liu XS, et al. (2012) Altitudinal variation in leaf construction cost and energy content of Bergenia purpurascens. Acta Oecologica 43: 72–79. DOI:10.1016/j.actao.2012.05.011.

    Article  Google Scholar 

  • Zhang S, Zhou Z, Hu H, et al. (2007) Gas exchange and resource utilization in two alpine oaks at different altitudes in the Hengduan Mountains. Canadian Journal of Forest Research 37: 1184–1193. DOI: 10.1139/X06-303.

    Article  Google Scholar 

  • Zhou Y, Schaub M, Shi L, et al. (2012) Non-linear response of stomata in Pinus koraiensis to tree age and elevation. Trees-Structure and Function 26: 1389–1396. DOI: 10.1007/s00468-012-0713-8.

    Article  Google Scholar 

  • 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/s00442-009-1515-6.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Key Laboratory of Mountain Surface Processes and Ecological Regulation, Institute of Mountain Hazards and Environment, Chinese Academy of Sciences, Chengdu, 610041, China

    Hong-xia Zhao, Bao-li Duan & Yan-bao Lei

Authors
  1. Hong-xia Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bao-li Duan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yan-bao Lei
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yan-bao Lei.

Additional information

0000-0002-8194-7700

0000-0002-0578-4663

0000-0003-1584-4874

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhao, Hx., Duan, Bl. & Lei, Yb. Causes for the unimodal pattern of leaf carbon isotope composition in Abies faxoniana trees growing in a natural forest along an altitudinal gradient. J. Mt. Sci. 12, 39–48 (2015). https://doi.org/10.1007/s11629-014-3174-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11629-014-3174-2

Keywords

Search

Navigation