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Age-related nutrient content and carbon isotope composition in the leaves and branches of Quercus aquifolioides along an altitudinal gradient

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Abstract

Quercus aquifolioides Rehder & E.H. Wilson, an evergreen alpine and subalpine species, occupies a wide range of habitats in the Wolong Nature Reserve, southwestern China. We measured age-related carbon (C) and nutrient (N, P, K, Mg and Ca) contents, C/N, carbon isotope composition (δ13C) and specific leaf area (SLA) in the leaves and branches of Q. aquifolioides trees along an altitudinal gradient ranging from 2,000 to 3,600 m. The results showed that both age and altitude significantly affected the morphological and physiological properties of Q. aquifolioides. Young tissues possessed higher contents of N, P, K and Mg, lower Ca contents, both on a dry mass basis (subscript “M”) and on a unit area basis (subscript “A”), and lower C/N and δ13C values than did the old ones. The levels of NM and δ13C increased with increasing altitude above 2,800 m, but decreased with increasing altitude below 2,800 m. In contrast, C/N and SLA showed opposite patterns, and other nutrient contents, including PM, KM, CaM and MgM, exhibited irregular changes with elevation. On the other hand, δ13C was positively correlated with NM in both leaves and branches, and negatively correlated with SLA in leaves along the altitudinal gradient. Our results also showed that both the MgM level of leaves and the CaM level of branches, besides the functional correlations between the NM level and the structure of leaves, are responsible for or accompanied by variation in δ13C. In addition, δ13C was negatively correlated with C/N in both leaves and branches along an altitudinal gradient. It follows that high-altitude plants achieve higher water use efficiency (WUE) at the expense of decreasing nitrogen use efficiency (NUE, derived from C/N), whereas plants at 2,800 m can maintain relatively higher NUE but lower WUE. These characteristics probably reflect the physiological potential of Q. aquifolioides for vigorous growth and metabolism at the optimum altitude (around 2,800 m). With increasing distance from the optimum altitude, NUE decreases. The observed intra-specific variation in the trade-off between WUE and NUE may partially explain the altitudinal distribution of Q. aquifolioides in relation to moisture and nutrient availability.

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References

  • Anderson JE, Williams J, Kriedemann PE, Austin MP, Farquhar GD (1996) Correlations between carbon isotope discrimination and climate of native habitats for diverse eucalypt taxa growing in a common garden. Aust J Plant Physiol 23:311–320

    Article  Google Scholar 

  • Atkinson CJ, Mansfield TA, Davies WJ (1990) Does calcium in xylem sap regulate stomatal conductance? New Phytol 116:19–27. doi:10.1111/j.1469-8137.1990.tb00506.x

    Article  CAS  Google Scholar 

  • Brandes E, Kodama N, Whittaker K, Weston C, Rennenberg H, Keitel C, Adams MA, Gessler A (2006) Short-term variation in the isotopic composition of organic matter allocated from the leaves to the stem of Pinus sylvestris: effects of photosynthetic and postphotosynthetic carbon isotope fractionation. Glob Chang Biol 12:1922–1939. doi:10.1111/j.1365-2486.2006.01205.x

    Article  Google Scholar 

  • Brodribb T, Hill RS (1998) The photosynthetic drought physiology of a diverse group of southern hemisphere conifer species is correlated with minimum seasonal rainfall. Funct Ecol 12:465–471. doi:10.1046/j.1365-2435.1998.00213.x

    Article  Google Scholar 

  • Chapin FS, Schulze ED, Mooney HA (1990) The ecology and economics of storage in plants. Annu Rev Ecol Syst 21:423–447. doi:10.1146/annurev.es.21.110190.002231

    Article  Google Scholar 

  • Chen S, Bai Y, Zhang L, Han X (2005) Comparing physiological responses of two dominant grass species to nitrogen addition in Xilin River Basin of China. Environ Exp Bot 53:65–75. doi:10.1016/j.envexpbot.2004.03.002

    Article  Google Scholar 

  • Chinese Soil Taxonomy Research Group ISSAS (1995) Chinese soil taxonomy (revised proposal). China Agricultural Scientech Press, Beijing (in Chinese)

    Google Scholar 

  • D’Alessandro CM, Guerrieri MR, Saracino A (2004) Comparing carbon isotope composition of bulk wood and holocellulose from Quercus cerris, Fraxinus ornus and Pinus radiata tree rings. Forest 1(1):51–57. doi:10.3832/efor0217-0010051

    Article  Google Scholar 

  • Damesin C, Lelarge C (2003) Carbon isotope composition of current-year shoots from Fagus sylvatica in relation to growth, respiration and use of reserves. Plant Cell Environ 26:207–219. doi:10.1046/j.1365-3040.2003.00951.x

    Article  Google Scholar 

  • Ehleringer JR, Cerling TE (1995) Atmospheric CO2 and the ratio of intercellular to ambient CO2 concentrations in plants. Tree Physiol 15:105–111

    PubMed  Google Scholar 

  • England JR, Attiwill PM (2006) Changes in leaf morphology and anatomy with tree age and height in the broad-leaved evergreen species, Eucalyptus regnans F. Muell. Trees (Berlin) 20:79–90. 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. J Ecol 91:880–889. doi:10.1046/j.1365-2745.2003.00818.x

    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 56:348–355. doi:10.1007/BF00379711

    Article  Google Scholar 

  • Flanagan LB, Johnsen KH (1995) Genetic variation in carbon isotope discrimination and its relationship to growth under field conditions in full-sib families of Picea mariana. Can J Res 25:39–47

    Article  Google Scholar 

  • Franco AC, Duarte HM, Geßler A, de Mattos EA, Nahm M, Rennenberg H, Ribeiro KT, Scarano FR, Lüttge U (2005) In situ measurements of carbon and nitrogen distribution and composition, photochemical efficiency and stable isotope ratios in Araucaria angustifolia. Trees Struct Funct 19:422–430

    CAS  Google Scholar 

  • Grassi G, Minotta G (2000) Influence of nutrient supply on shade–sun acclimation of Picea abies seedlings: effects on foliar morphology, photosynthetic performance and growth. Tree Physiol 20:645–652

    PubMed  Google Scholar 

  • Hamerlynck EP, Huxman TE, McAuliffe JR, Smith SD (2004) Carbon isotope discrimination and foliar nutrient status of Larrea tridentata (creosote bush) in contrasting Mojave desert soils. Oecologia 138:210–215. doi:10.1007/s00442-003-1437-7

    Article  PubMed  Google Scholar 

  • Hobbie EA, Werner RA (2004) Intramolecular, compound-specific, and bulk carbon isotope patterns in C3 and C4 plants: a review and synthesis. New Phytol 161:371–385. doi:10.1111/j.1469-8137.2004.00970.x

    Article  CAS  Google Scholar 

  • Hubick KT, Farquhar GD, Shorter R (1986) Correlation between water-use efficiency and carbon isotope discrimination in diverse peanut (Arachis) germplasm. Aust J Plant Physiol 13:803–816

    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 

  • Körner C, Larcher W (1988) Plant life in cold climates. Symp Soc Exp Biol 42:25–57

    PubMed  Google Scholar 

  • Körner C, Farquhar GD, Roksandic Z (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 plants follows latitudinal and altitudinal trends. Oecologia 88:30–40. doi:10.1007/BF00328400

    Article  Google Scholar 

  • Laclau JP, Bouillet JP, Ranger J, Joffre R, Gouma R, Saya A (2001) Dynamics of nutrient translocation in stemwood across an age series of a eucalyptus hybrid. Ann Bot 88:1079–1092. doi:10.1006/anbo.2001.1550

    Article  CAS  Google Scholar 

  • Leegood RC, Walker DA, Foyer CH (1986) Regulation of the Benson–Calvin cycle. In: Barber J, Baker NR (eds) Photosynthetic mechanisms and the environment. Elsevier, Amsterdam, pp 189–258

    Google Scholar 

  • Li C, Liu S, Berninger F (2004) Picea seedlings show apparent acclimation to drought with increasing altitude in the eastern Himalaya. Trees Struct Funct 18:277–283. doi:10.1007/s00468-003-0304-9

    Article  Google Scholar 

  • Li C, Zhang X, Liu X, Luukkanen O, Berninger F (2006) Leaf morphological and physiological responses of Quercus aquifolioides along an altitudinal gradient. Silva Fenn 40:5–13

    Google Scholar 

  • Liu G, Zhao S, Wang H, Tu X (2001) Nutrient distribution for non-photosynthetic organs in the sharp-tooth oak stands. Acta Ecol Sin 21:422–429

    Google Scholar 

  • Liu XL, Hao XD, Yang DS, Liu SR, Su YM, Cai XH, He F, Ma QY (2006) Aboveground biomass and its models of Quercus aquifolioides thicket community in Balangshan Mountain in Wolong Natural Reserve. Chin J Ecol 25:487–491

    Google Scholar 

  • Livingston NJ, Guy RD, Sun ZJ, 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 Environ 22:281–289. doi:10.1046/j.1365-3040.1999.00400.x

    Article  Google Scholar 

  • Lloyd J, Syvertsen JP, Kriedemann PE, Farquhar GD (1992) Low conductances for CO2 diffusion from stomata to the sites of carboxylation in leaves of woody species. Plant Cell Environ 15:873–899. doi:10.1111/j.1365-3040.1992.tb01021.x

    Article  CAS  Google Scholar 

  • Major JE, Barsi DC, Mosseler A, Campbell M (2007) Genetic variation and control of chloroplast pigment content in Picea rubens, Picea mariana, and their hybrids. 1. Under ambient and elevated CO2 environments. Tree Physiol 27:353–364

    PubMed  CAS  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants. Academic Press, London

    Google Scholar 

  • Marshall JD, Zhang J (1994) Carbon isotope discrimination and water-use efficiency in native plants of the North-Central Rockies. Ecology 75:1887–1895. doi:10.2307/1941593

    Article  Google Scholar 

  • Miller HG, Cooper JM, Mille JD, Pauline OJL (1979) Nutrient cycles in pine and their adaptation to poor soils. Can J Res 9:19–26. doi:10.1139/x79-004

    Article  Google Scholar 

  • Mitchell AK (1998) Acclimation of Pacific yew (Taxus brevifolia) foliage to sun and shade. Tree Physiol 18:749–775

    PubMed  Google Scholar 

  • Nelson DW, Sommers LE (1982) Total carbon, organic carbon and organic matter. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis, Part 2. American Society of Agronomy and Soil Science, Madison, pp 539–579

    Google Scholar 

  • Panek JA, Waring RH (1995) Carbon isotope variation in Douglas fir foliage: improving the δ13C–climate relationship. Tree Physiol 15:657–663

    PubMed  Google Scholar 

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

    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 Environ 29:823–835. doi:10.1111/j.1365-3040.2005.01452.x

    Article  PubMed  CAS  Google Scholar 

  • Rebeille F, Bligny R, Martin JB, Douce R (1983) Relationship between the cytoplasm and the vacuole phosphate pool in Acer pseudoplatanus cells. Arch Biochem Biophys 225:143–148. doi:10.1016/0003-9861(83)90017-6

    Article  PubMed  CAS  Google Scholar 

  • Saur E, Nambiar EK, Fife DN (2000) Foliar nutrient retranslocation in Eucalyptus globulus. Tree Physiol 20:1105–1112

    PubMed  CAS  Google Scholar 

  • Saurer M, Maurer S, Matyssek R, Landolt W, Günthardt-Goerg MS, Siegenthaler U (1995) The influence of ozone and nutrition on δ13C in Betula pendula. Oecologia 103:397–406. doi:10.1007/BF00328677

    Article  Google Scholar 

  • Scartazza A, Mata C, Matteucci G, Yakir D, Moscatello S, Brugnoli E (2004) Comparisons of δ13C of photosynthetic products and ecosystem respiratory CO2 and their responses to seasonal climate variability. Oecologia 140:340–351. doi:10.1007/s00442-004-1588-1

    Article  PubMed  Google Scholar 

  • Scheiner SM, Goodnight CJ (1984) The comparison of phenotypic plasticity and genetic variation in populations of the grass Danthonia spicata. Evol Int J Org Evol 38:845–855. doi:10.2307/2408395

    Google Scholar 

  • Shen Z, Liu Y (1998) The regional characteristic of the forest community superior stand nutrient element content in China. J Hubei Inst Nationalities 16:30–32

    Google Scholar 

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

    Article  Google Scholar 

  • Sun ZJ, Livingston NJ, Guy RD, Ethier GJ (1996) Stable carbon isotopes as indicators of increased water use efficiency and productivity in white spruce (Picea glauca (Moench) Voss) seedlings. Plant Cell Environ 19:887–894. doi:10.1111/j.1365-3040.1996.tb00425.x

    Article  Google Scholar 

  • Takagi S, Nagai R (1992) Several aspects of current research into the role of calcium in plant physiology. Bot Mag 105:687–697. doi:10.1007/BF02489443

    Article  CAS  Google Scholar 

  • Tegischer K, Tausz M, Wieser G, Grill D (2002) Tree- and needle-age-dependent variations in antioxidants and photoprotective pigments in Norway spruce needles at the alpine timberline. Tree Physiol 22:591–596

    PubMed  CAS  Google Scholar 

  • Terwilliger VJ, Kitajima K, Le Roux-Swarthout DJ, Mulkey S, Wright SJ (2001) Intrinsic water-use efficiency and heterotrophic investment in tropical leaf growth of two neotropical pioneer tree species as estimated from δ13C values. New Phytol 152:267–281. doi:10.1046/j.0028-646X.2001.00252.x

    Article  Google Scholar 

  • Tsialtas JT, Maslaris N (2006) Leaf carbon isotope discrimination relationships to element content in soil, roots and leaves of sugar beets grown under Mediterranean conditions. Field Crops Res 99:125–135. doi:10.1016/j.fcr.2006.04.004

    Article  Google Scholar 

  • Wang GG, Klinka K (1997) White spruce foliar nutrient concentrations in relation to tree growth and soil nutrient amounts. For Ecol Manage 98:89–99

    Article  Google Scholar 

  • Wang JR, Zhong AL, Simard SW, Kimmins JP (1996) Aboveground biomass and nutrient accumulation in an age sequence of paper birch (Betula papyrifera) in the Interior Cedar Hemlock zone, British Columbia. For Ecol Manage 83:27–38

    Article  Google Scholar 

  • Weih M (2001) Evidence for increased sensitivity to nutrient and water stress in a fast-growing hybrid willow compared with a natural willow clone. Tree Physiol 21:1141–1148

    PubMed  CAS  Google Scholar 

  • Woodward FI (1986) Ecophysiological studies on the shrub Vaccinium myrtillus L. taken from a wide altitudinal range. Oecologia 70:580–586. doi:10.1007/BF00379908

    Article  Google Scholar 

  • Wright IJ, Reich PB, Westoby M (2001) Strategy shifts in leaf physiology, structure and nutrient content between species of high- and low-rainfall and high- and low-nutrient habitats. Funct Ecol 15:423–434. doi:10.1046/j.0269-8463.2001.00542.x

    Article  Google Scholar 

  • Xu RQ, Guan ZT (1992) Quercus aquifolioides forest. In: Yang YP (ed) Forests in Sichuan. China Forestry Press, Beijing, pp 634–645 (In Chinese)

    Google Scholar 

  • Xu ZH, Saffigna PG, Farquhar GD, Simpson JA, Haines RJ, Walker S, Osborne DO, Guinto D (2000) Carbon isotope discrimination and oxygen isotope composition in clones of the F (1) hybrid between slash pine and Caribbean pine in relation to tree growth, water-use efficiency and foliar nutrient concentration. Tree Physiol 20:1209–1217

    PubMed  CAS  Google Scholar 

  • Xu ZH, Prasolova NV, Lundkvist K, Beadle C, Leaman T (2003) Genetic variation in carbon and nitrogen isotope composition and nutrient concentration in the foliage of 10-year-old hoop pine families in relation to tree growth in subtropical Australia. For Ecol Manage 186:359–371

    Article  Google Scholar 

  • Yang QZ (1990) The characteristics and classification of oak durisilvae in the Himalayan region of China. Acta Phytoecol Geobot Sin 14:197–211 In Chinese

    Google Scholar 

  • Zas R, Serrada R (2003) Foliar nutrient status and nutritional relationships of young Pinus radiata D. Don plantations in northwest Spain. For Ecol Manage 174:167–176

    Article  Google Scholar 

  • Zhang X, Korpelainen H, Li C (2006) Microsatellite variation of Quercus aquifolioides populations at varying altitudes in the Wolong natural reserve of China. Silva Fenn 40:407–415

    Google Scholar 

  • Zhou LJ, Guan ZT (1992) Quercus aquifolioides thicket forests. In: Yang YP (ed) The forests in Sichuan. China Forestry Press, Beijing, pp 736–741 (In Chinese)

    Google Scholar 

  • Ziegler H (1995) Stable isotopes in plant physiology and ecology. Prog Bot 56:1–24

    CAS  Google Scholar 

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Acknowledgments

The research was supported by the Program of “Knowledge Innovation Engineering” of the Chinese Academy of Sciences (No. KSCX2-YW-N-064) and the Outstanding Young Scientist Program of the National Science Foundation of China (No. 30525036).

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Correspondence to Chunyang Li.

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

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