Skip to main content
Log in

Age-related changes of leaf traits and stoichiometry in an alpine shrub (Rhododendron agglutinatum) along altitudinal gradient

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

An Erratum to this article was published on 02 March 2017

Abstract

Leaf morphological and stoichiometric characteristics are considered to represent both the interior inheritable characters in the plant and its adaptations to specific exterior environments. Rhododendron agglutinatum, an evergreen alpine shrub species, occupies a wide range of habitats above timberline in the Miyaluo Natural Reserve, southwestern China. Along an altitudinal gradient ranging from 3700 to 4150 m, we measured leaf morphological characters including leaf dry matter content (LDMC), leaf dry mass per unit area (LMA), and one leaf area (OLA), as well as carbon (C) and nutrient (N, P) contents in leaves of three different age groups (juvenile leaves, mature leaves and senescent leaves). We also calculated the stoichiometric relationships among carbon and nutrients (C/N, C/P and N/P). Results showed that both age and altitude affected the leaf morphological and stoichiometric properties of R. agglutinatum. Mature leaves possessed the highest LDMC, LMA and C contents both on a dry mass basis and on a unit area basis. Younger leaves possessed higher contents of nutrients. OLA as well as ratios between carbon and nutrients (C/N, C/P) increased with ages. Juvenile leaves possessed lowest ratio between nitrogen and phosphorus. In juvenile leaves, nutrients increased with altitudinal elevation, whereas other traits decreased. In mature leaves, nutrients and their ratios with carbon showed consistent trends with juvenile leaves along increasing altitude, whereas LMA and carbon on a unit area basis showed opposite trends with juvenile leaves along increasing altitude. In senescent leaves, only content of phosphorus on a unit area basis and N/P were found linearly correlated with altitude. Our results demonstrated a clear pattern of nutrient distribution with aging process in leaves and indicated that a high possibility of N limitation in this region. We also concluded that younger leaves could be more sensitive to climate changes due to a greater altitudinal influence on the leaf traits in younger leaves than those in elder leaves.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Ackerly DD, Knight CA, Weiss SB, et al. (2002) Leaf size, specific leaf area and microhabitat distribution of chaparral woody plants: contrasting patterns in species level and community level analyses. Oecologia 130(3): 449–457.

    Article  Google Scholar 

  • Chapin FS, Schulze ED, Mooney HA (1990) The Ecology and Economics of Storage in Plants. Annual Review of Ecology and Systematics 21: 423–447. DOI: 10.1146/annurev.es.21.110190.002231

    Article  Google Scholar 

  • Chen B, Liu S, Ge J, et al. (2010) Annual and seasonal variations of Q10 soil respiration in the sub-alpine forests of the Eastern Qinghai-Tibet Plateau, China. Soil Biology and Biochemistry 42(10): 1735–1742. DOI: 10.1016/j.soilbio.2010.06.010

    Article  Google Scholar 

  • Chen SP, Bai YF, Zhang LX, et al. (2005) Comparing physiological responses of two dominant grass species to nitrogen addition in Xilin River Basin of China. Environmental and Experimental Botany 53(1): 65–75. DOI: 10.1016/j.envexpbot.2004.03.002

    Article  Google Scholar 

  • Cordell S, Goldstein G, Meinzer FC, et al. (1999) Allocation of nitrogen and carbon in leaves of Metrosideros polymorpha regulates carboxylation capacity and delta C-13 along an altitudinal gradient. Functional Ecology 13(6): 811–818. DOI: 10.1046/j.1365-2435.1999.00381.x

    Article  Google Scholar 

  • Day ME, Greenwood MS, White AS (2001) Age-related changes in foliar morphology and physiology in red spruce and their influence on declining photosynthetic rates and productivity with tree age. Tree Physiology 21(16): 1195–1204. DOI: 10.1093/treephys/21.16.1195

    Article  Google Scholar 

  • England JR, Attiwill PM (2006) Changes in leaf morphology and anatomy with tree age and height in the broadleaved evergreen species, Eucalyptus regnans F. Muell. Trees-Structure and Function 20(1): 79–90. DOI: 10.1007/s00468-005-0015-5

    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(5): 880–889. DOI: 10.1046/j.1365-2745.2003.00818.x

    Article  Google Scholar 

  • Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78(1): 9–19. DOI: 10.1007/bf00377192

    Article  Google Scholar 

  • Fajardo A, Piper FI, Pfund L, et al. (2012) Variation of mobile carbon reserves in trees at the alpine treeline ecotone is under environmental control. New Phytologist 195(4): 794–802. DOI: 10.1111/j.1469-8137.2012.04214.x

    Article  Google Scholar 

  • Field C (1983) Allocating Leaf Nitrogen for the Maximization of Carbon Gain-Leaf Age as a Control on the Allocation Program. Oecologia 56(2–3): 341–347. DOI: 10.1007/BF00379710

    Article  Google Scholar 

  • Field C, Mooney HA (1983) Leaf Age and Seasonal Effects on Light, Water, and Nitrogen Use Efficiency in a California Shrub. Oecologia 56(2–3): 348–355. DOI: 10.1007/BF00379711

    Article  Google Scholar 

  • Friend AD, Woodward FI (1990) Evolutionary and Ecophysiological Responses of Mountain Plants to the Growing Season Environment. Advances in Ecological Research. A. H. F. M. Begon and A. Macfadyen, Academic Press. Volume 20: 59–124.

    Google Scholar 

  • Grime JP, Thompson K, Hunt R, et al. (1997) Integrated screening validates primary axes of specialisation in plants. Oikos 79(2): 259–281. DOI: 10.2307/3546011

    Article  Google Scholar 

  • Harper JL (1989) The Value of a Leaf. Oecologia 80(1): 53–58. DOI: 10.1007/BF00789931

    Article  Google Scholar 

  • He JS, Fang JY, Wang ZH, et al. (2006a) Stoichiometry and large-scale patterns of leaf carbon and nitrogen in the grassland biomes of China. Oecologia 149(1): 115–122. DOI: 10.1007/s00442-006-0425-0

    Article  Google Scholar 

  • He JS, Wang L, Flynn DFB, et al. (2008) Leaf nitrogen: phosphorus stoichiometry across Chinese grassland biomes. Oecologia 155(2): 301–310. DOI: 10.1007/s00442-007-0912-y

    Article  Google Scholar 

  • He JS, Wang ZH, Wang XP, et al. (2006b) A test of the generality of leaf trait relationships on the Tibetan Plateau. New Phytologist 170(4): 835–848. DOI: 10.1111/j.1469-8137.2006.01704.x

    Article  Google Scholar 

  • Hedin LO (2004) Global organization of terrestrial plantnutrient interactions. Proceedings of the National Academy of Sciences of the United States of America 101(30): 10849–10850. DOI: 10.1073/pnas.0404222101

    Article  Google Scholar 

  • 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(1): 121–150. DOI: 10.1023/A:102602021 0887

    Article  Google Scholar 

  • Hultine KR, Marshall JD (2000) Altitude trends in conifer leaf morphology and stable carbon isotope composition. Oecologia 123(1): 32–40. DOI: 10.1007/s004420050986

    Article  Google Scholar 

  • Körner C (1989) The Nutritional-Status of Plants from High-Altitudes-a Worldwide Comparison. Oecologia 81(3): 379–391. DOI: 10.1007/BF00377088

    Article  Google Scholar 

  • Körner C (1998) A re-assessment of high elevation treeline positions and their explanation. Oecologia 115(4): 445–459. DOI: 10.1007/s004420050540

    Article  Google Scholar 

  • Körner C (2003) Alpine Plant Life: Functional Plant Ecology of High Mountain Ecosystems Berlin Heidelberg, Springer

  • Körner 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. DOI: 10.2307/2389420

    Article  Google Scholar 

  • Körner C, Larcher W (1988) Plant Life in Cold Climates. Symposia of the Society for Experimental Biology 42: 25–57.

    Google Scholar 

  • Körner C, Neumayer M, Menendezriedl SP, et al. (1989) Functional-Morphology of Mountain Plants. Flora 182(5–6): 353–383.

    Article  Google Scholar 

  • Klich MG (2000) Leaf variations in Elaeagnus angustifolia related to environmental heterogeneity. Environmental and Experimental Botany 44(3): 171–183. DOI: 10.1016/S0098-8472(00)00056-3

    Article  Google Scholar 

  • Koerselman W, Meuleman AFM (1996) The vegetation N:P ratio: A new tool to detect the nature of nutrient limitation. Journal of Applied Ecology 33(6): 1441–1450. DOI: 10.2307/2404783

    Article  Google Scholar 

  • Laclau JP, Bouillet JP, Ranger J, et al. (2001) Dynamics of nutrient translocation in stemwood across an age series of a eucalyptus hybrid. Annals of Botany 88(6): 1079–1092. DOI: 10.1006/anbo.2001.1550

    Article  Google Scholar 

  • Lambers H, Raven JA, Shaver GR, et al. (2008) Plant nutrientacquisition strategies change with soil age. Trends in Ecology & Evolution 23(2): 95–103. DOI: 10.1016/j.tree.2007.10.008

    Article  Google Scholar 

  • Li CY, Wu CC, Duan BL, et al. (2009a) 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(5): 1109–1121. DOI: 10.1007/s00468-009-0354-8

    Article  Google Scholar 

  • Li MC, Kong GQ, Zhu JJ (2009b) Vertical and leaf-age-related variations of nonstructural carbohydrates in two alpine timberline species, southeastern Tibetan Plateau. Journal of Forest Research 14(4): 229–235. DOI: 10.1007/s10310-009-0132-x

    Article  Google Scholar 

  • Li MH, Hoch G, Körner C (2001) Spatial variability of mobile carbohydrates within Pinus cembra trees at the alpine treeline. Phyton-Annales Rei Botanicae 41(2): 203–213.

    Google Scholar 

  • Li MH, Hoch G, Körner C (2002) Source/sink removal affects mobile carbohydrates in Pinus cembra at the Swiss treeline. Trees-Structure and Function 16(4–5): 331–337. DOI: 10.1007/s00468-002-0172-8

    Article  Google Scholar 

  • Li MH, Xiao WF, Shi PL, et al. (2008a) Nitrogen and carbon source-sink relationships in trees at the Himalayan treelines compared with lower elevations. Plant Cell and Environment 31(10): 1377–1387. DOI: 10.1111/j.1365-3040.2008.01848.x

    Article  Google Scholar 

  • Li MH, Xiao WF, Wang SG, et al. (2008b) Mobile carbohydrates in Himalayan treeline trees I. Evidence for carbon gain limitation but not for growth limitation. Tree Physiology 28(8): 1287–1296. DOI: 10.1093/treephys/28.8. 1287

    Google Scholar 

  • Livingston NJ, Guy RD, Sun ZJ, et al. (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(3): 281–289. DOI: 10.1046/j.1365-3040.1999.00400.x

    Article  Google Scholar 

  • Luo SZ, Liu GH, Li ZS, et al. (2014) Soil respiration along an altitudinal gradient in a subalpine secondary forest in China. Iforest-Biogeosciences and Forestry 8: 526–532. DOI: 10.3832 /ifor0895-007

    Article  Google Scholar 

  • McGroddy ME, Daufresne T, Hedin LO (2004) Scaling of C: N: P stoichiometry in forests worldwide: Implications of terrestrial redfield-type ratios. Ecology 85(9): 2390–2401. DOI: 10.1890/03-0351

    Article  Google Scholar 

  • Miller HG, Cooper JM, Miller JD, et al. (1979) Nutrient Cycles in Pine and Their Adaptation to Poor Soils. Canadian Journal of Forest Research-Revue Canadienne De Recherche Forestiere 9(1): 19–26. DOI: 10.1139/x79-004

    Article  Google Scholar 

  • Niinemets U (2002) Stomatal conductance alone does not explain the decline in foliar photosynthetic rates with increasing tree age and size in Picea abies and Pinus sylvestris. Tree Physiology 22(8): 515–535. DOI: 10.1093/treephys/22.8.515

    Article  Google Scholar 

  • Niklas KJ (2006) Plant allometry, leaf nitrogen and phosphorus stoichiometry, and interspecific trends in annual growth rates. Annals of Botany 97(2): 155–163. DOI: 10.1093/aob/mcj021

    Article  Google Scholar 

  • Niklas KJ, Owens T, Reich PB, et al. (2005) Nitrogen/phosphorus leaf stoichiometry and the scaling of plant growth. Ecology Letters 8(6): 636–642. DOI: 10.1111/j.1461-0248.2005.00759.x

    Article  Google Scholar 

  • Patterson TB, Guy RD, Dang QL (1997) Whole-plant nitrogenand water-relations traits, and their associated trade-offs, in adjacent muskeg and upland boreal spruce species. Oecologia 110(2): 160–168. DOI: 10.1007/s004420050145

    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(3): 565–588. DOI: 10.1111/j.1469-8137.2009.02830.x

    Article  Google Scholar 

  • Reich PB, Ellsworth DS, Walters MB, et al. (1999) Generality of leaf trait relationships: A test across six biomes. Ecology 80(6): 1955–1969. DOI: 10.1890/0012-9658(1999)080 [1955: GOLTRA]2.0.CO;2

    Article  Google Scholar 

  • Reich PB, Oleksyn J (2004) Global patterns of plant leaf N and P in relation to temperature and latitude. Proceedings of the National Academy of Sciences of the United States of America 101(30): 11001–11006. DOI: 10.1073/pnas.0403588101

    Article  Google Scholar 

  • Rijkers T, Pons TL, Bongers F (2000) The effect of tree height and light availability on photosynthetic leaf traits of four neotropical species differing in shade tolerance. Functional Ecology 14(1): 77–86. DOI: 10.1046/j.1365-2435.2000.00395.x

    Article  Google Scholar 

  • Saur E, Nambiar EKS, Fife DN (2000) Foliar nutrient retranslocation in Eucalyptus globulus. Tree Physiology 20(16): 1105–1112. DOI: 10.1093/treephys/20.16.1105

    Article  Google Scholar 

  • Saura-Mas S, Lloret F (2007) Leaf and shoot water content and leaf dry matter content of Mediterranean woody species with different post-fire regenerative strategies. Annals of Botany 99(3): 545–554. DOI: 10.1093/aob/mcl284

    Article  Google Scholar 

  • Scheiner SM, Goodnight CJ (1984) The Comparison of Phenotypic Plasticity and Genetic Variation in Populations of the Grass Danthonia spicata. Evolution 38(4): 845–855. DOI: 10.2307/2408395

    Article  Google Scholar 

  • Sparks JP, Ehleringer JR (1997) Leaf carbon isotope discrimination and nitrogen content for riparian trees along elevational transects. Oecologia 109(3): 362–367. DOI: 10.1007/s004420050094

    Article  Google Scholar 

  • Steele MJ, Coutts MP, Yeoman MM (1989) Developmental-Changes in Sitka Spruce as Indexes of Physiological Age.1. Changes in Needle Morphology. New Phytologist 113(3): 367–375. DOI: 10.1111/j.1469-8137.1989.tb02415.x

    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 & Environment 27(8): 1047–1054. DOI: 10.1111/j.1365-3040.2004.01209.x

    Article  Google Scholar 

  • Tegischer K, Tausz M, Wieser G, et al. (2002) Tree-and needleage-dependent variations in antioxidants and photoprotective pigments in Norway spruce needles at the alpine timberline. Tree Physiology 22(8): 591–596. DOI: 10.1093/treephys/22.8.591

    Article  Google Scholar 

  • Tessier JT, Raynal DJ (2003) Use of nitrogen to phosphorus ratios in plant tissue as an indicator of nutrient limitation and nitrogen saturation. Journal of Applied Ecology 40(3): 523–534. DOI: 10.1046/j.1365-2664.2003.00820.x

    Article  Google Scholar 

  • Vendramini F, Diaz S, Gurvich DE, et al. (2002) Leaf traits as indicators of resource-use strategy in floras with succulent species. New Phytologist 154(1): 147–157. DOI: 10.1046/j. 1469-8137.2002.00357.x

    Article  Google Scholar 

  • Wang GG, Klinka K (1997) White spruce foliar nutrient concentrations in relation to tree growth and soil nutrient amounts. Forest Ecology and Management 98(1): 89–99. DOI: 10.1016/S0378-1127(97)00048-0

    Article  Google Scholar 

  • Wang JR, Zhong AL, Simard SW, et al. (1996) Aboveground biomass and nutrient accumulation in an age sequence of paper birch (Betula papyrifera) in the Interior Cedar Hemlock Zone, British Columbia. Forest Ecology and Management 83(1–2): 27–38. DOI: 10.1016/0378-1127(96)03703-6

    Article  Google Scholar 

  • Weih M, Karlsson PS (2001) Growth response of Mountain birch to air and soil temperature: is increasing leaf-nitrogen content an acclimation to lower air temperature? New Phytologist 150(1): 147–155. DOI: 10.1046/j.1469-8137.2001. 00078.x

    Article  Google Scholar 

  • Westoby M, Warton D, Reich PB (2000) The time value of leaf area. American Naturalist 155(5): 649–656. DOI: 10.1086/303346

    Article  Google Scholar 

  • Wright IJ, Reich PB, Westoby M, et al. (2004) The worldwide leaf economics spectrum. Nature 428(6985): 821–827. DOI: 10.1038/nature02403

    Article  Google Scholar 

  • Wu TG, Yu MK, Wang GG, et al. (2012) Leaf nitrogen and phosphorus stoichiometry across forty-two woody species in Southeast China. Biochemical Systematics and Ecology 44: 255–263. DOI: 10.1016/j.bse.2012.06.002

    Article  Google Scholar 

  • Xu M, Wang G, Li X, et al. (2015) The key factor limiting plant growth in cold and humid alpine areas also plays a dominant role in plant carbon isotope discrimination. Frontiers in Plant Science 6. DOI: 10.3389/fpls.2015.00961

  • Yoder BJ, Ryan MG, Waring RH, et al. (1994) Evidence of Reduced Photosynthetic Rates in Old Trees. Forest Science 40(3): 513–527.

    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(1–3): 167–176. DOI: 10.1016/S0378-1127(02)00027-0

    Article  Google Scholar 

  • Zhang SB, Zhang JL, Slik JWF, et al. (2012) Leaf element concentrations of terrestrial plants across China are influenced by taxonomy and the environment. Global Ecology and Biogeography 21(8): 809–818. DOI: 10.1111/j.1466-8238.2011.00729.x

    Article  Google Scholar 

  • Zhou HR, Xu M, Pan HL, et al. (2015) Leaf-age effects on temperature responses of photosynthesis and respiration of an alpine oak, Quercus aquifolioides, in southwestern China. Tree Physiology 35(11): 1236–1248. DOI: 10.1093/treephys/tpv101

    Article  Google Scholar 

  • Zhu B, Wang X, Fang J, et al. (2010) Altitudinal changes in carbon storage of temperate forests on Mt Changbai, Northeast China. Journal of Plant Research 123(4): 439–452. DOI: 10.1007/s10265-009-0301-1

    Article  Google Scholar 

Download references

Acknowledgement

This study was supported by the National Natural Science Foundation of China (No. 41071039) and National Key Research and Development Program (No. 2016YFC0502100).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Guo-hu Liu.

Additional information

http://orcid.org/0000-0001-8847-4398

http://orcid.org/0000-000-5423-1109

http://orcid.org/0000-0002-8106-4561

http://orcid.org/0000-0003-1251-5012

http://orcid.org/0000-0003-1547-9790

http://orcid.org/0000-0002-6134-7791

http:/orcid.org/0000-0003-0784-2270

An erratum to this article is available at http://dx.doi.org/10.1007/s11629-016-4080-6.

Electronic supplementary material

11629_2016_4096_MOESM1_ESM.pdf

Age-related changes of leaf traits and stoichiometry in an alpine shrub (Rhododendron agglutinatum) along altitudinal gradient

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, M., Liu, Gh., Jin, Tt. et al. Age-related changes of leaf traits and stoichiometry in an alpine shrub (Rhododendron agglutinatum) along altitudinal gradient. J. Mt. Sci. 14, 106–118 (2017). https://doi.org/10.1007/s11629-016-4096-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11629-016-4096-y

Keywords

Navigation