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Carbon and nitrogen stable isotope signals for an entire alpine flora, based on herbarium samples

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Abstract

Stable carbon and nitrogen isotopes provide time-integrated signals of plant carbon and nitrogen relations. We assessed an entire alpine flora in the Swiss Alps at ca. 2400 m elevation, using year 2007 herbarium samples of 245 species, 141 genera and 42 families to explore functional trait diversity. Despite overall similar macro-environmental conditions (moisture, soils, elevation), signal variation covered the full spectrum known for C3 plants. Variation among means for plant families for both δ13C and δ15N was smaller than variation among species within families. Species identity was of far greater importance than family affiliation. Similarly, tissue nitrogen and carbon concentrations varied in a rather species-specific manner, not permitting any a priori plant functional group definition based on such traits. The study also yielded tissue-type specificity of isotope signals. The elevation signal in δ13C (known to be less negative at high elevation) was much less pronounced than observed previously in con-generic comparisons. Thus, elevational δ13C trends are hard to distinguish from species effects in mixed populations over narrow ranges of elevation. δ15N data offer more space for ecological interpretation and show family specificity of signals in few cases. Cyperaceae, the most prominent family in this region, show no discrimination against 15N (like Fabaceae) and must have access to N sources different from most other families. This deserves experimental clarification, given the significance of Cyperaceae in cold environments. Overall, our study evidenced very high functional diversity among alpine plant species, as captured by these isotope signals.

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References

  • Amundson R, Austin AT, Schuur EAG, Yoo K, Matzek V, Kendall C, Uebersax A, Brenner D, Baisden WT (2003) Global patterns of the isotopic composition of soil and plant nitrogen. Global Biogeochem Cycles 17:1031

    Article  Google Scholar 

  • Bowman WD, Schardt JC, Schmidt SK (1996) Symbiotic N-2-fixation in alpine tundra: ecosystem input and variation in fixation rates among communities. Oecologia 108:345–350

    Article  Google Scholar 

  • Casper BB, Goldman R, Lkhagva A, Helliker BR, Plante AF, Spence LA, Liancourt P, Boldgiv B, Petraitis PS (2012) Legumes mitigate ecological consequences of a topographic gradient in a northern Mongolian steppe. Oecologia 169:85–94

    Article  PubMed  Google Scholar 

  • Chalk PM, Smith CJ, Hopmans P, Hamilton SD (1996) A yield-independent, N-15-isotope dilution method to estimate legume symbiotic dependence without a non-N-2-fixing reference plant. Biol Fertil Soils 23:196–199

    Article  CAS  Google Scholar 

  • Chapin FS, Moilanen L, Kielland K (1993) Preferential use of organic nitrogen for growth by a nonmycorrhizal arctic sedge. Nature 361:150–153

    Article  CAS  Google Scholar 

  • Chevillat VS, Siegwolf RTW, Pepin S, Körner C (2005) Tissue-specific variation of delta 13-C in mature canopy in a temperate forest in central Europe. Basic Appl Ecol 6:519–534

    Article  Google Scholar 

  • Craine JM, Elmore AJ, Aidar MPM, Bustamante M, Dawson TE, Hobbie EA, Kahmen A, Mack MC, McLauchlan KK, Michelsen A, Nardoto GB, Pardo LH, Penuelas J, Reich PB, Schuur EAG, Stock WD, Templer PH, Virginia RA, Welker JM, Wright IJ (2009) Global patterns of foliar nitrogen isotopes and their relationships with climate, mycorrhizal fungi, foliar nutrient concentrations, and nitrogen availability. New Phytol 183:980–992

    Article  CAS  PubMed  Google Scholar 

  • Cripps CL, Eddington LH (2005) Distribution of mycorrhizal types among alpine vascular plant families on the Beartooth Plateau, rocky mountains, USA, in reference to large-scale patterns in arctic-alpine habitats. Arct Antarct Alp Res 37:177–188

    Article  Google Scholar 

  • Downton WJS, Grant WJR, Robinson SP (1985) Photosynthetic and stomatal responses of spinach leaves to salt stress. Plant Physiol 78:85–88

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Falkengren-Grerup U, Lakkenborg-Kristensen H (1994) Importance of ammonium and nitrate to the performance of herb-layer species from deciduous forest herbs and grasses. Environ Exp Bot 34:31–38

    Article  Google Scholar 

  • Farquhar GD, Von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90

    Article  CAS  PubMed  Google Scholar 

  • Farquhar GD, Oleary MH, Berry JA (1982) On the relationship between carbon isotope discrimination and the inter-cellular carbon-dioxide concentration in leaves. Austral J Plant Phys 9:121–137

    Article  CAS  Google Scholar 

  • Garten CT (1993) Variation in foliar N-15 abundance and the availability of soil-nitrogen on Walker Branch watershed. Ecology 74:2098–2113

    Article  Google Scholar 

  • Gathumbi SM, Cadisch G, Giller KE (2002) N-15 natural abundance as a tool for assessing N-2-fixation of herbaceous, shrub and tree legumes in improved fallows. Soil Biol Biochem 34:1059–1071

    Article  CAS  Google Scholar 

  • Gebauer G, Dietrich P (1993) Nitrogen isotope ratios in different compartments of a mixed stand of spruce, larch and beech trees and of understory vegetation including fungi. Isotopenpraxis 29:35–44

    CAS  Google Scholar 

  • Gigon A, Rorison IH (1972) Response of some ecologically distinct plant species to nitrate-nitrogen and to ammonium-nitrogen. J Ecol 60:93–102

    Article  CAS  Google Scholar 

  • Giller KE, Ormesher J, Awah FM (1991) Nitrogen transfer from Phaseolus bean to intercropped maize measured using 15N-enrichment and 15N-isotope dilution methods. Soil Biol Biochem 23:339–346

    Article  CAS  Google Scholar 

  • Handley LL, Raven JA (1992) The use of natural abundance of nitrogen isotopes in plant physiology and ecology. Plant Cell Env 15:965–985

    Article  CAS  Google Scholar 

  • Handley LL, Azcon R, Lozano JMR, Scrimgeour CM (1999) Plant delta N-15 associated with arbuscular mycorrhization, drought and nitrogen deficiency. Rapid Comm Mass Spectrometry 13:1320–1324

    Article  CAS  Google Scholar 

  • Haselwandter K (1987) Mycorrhizal infection and its possible ecological significance in climatically and nutritionally stressed alpine plant-communities. Angewandte Botanik 61:107–114

    Google Scholar 

  • Haynes RJ, Goh KM (1978) Ammonium and nitrate nutrition of plants. Biol Rev Camb Philos 53:465–510

    Article  CAS  Google Scholar 

  • Hefel C, Stoecklin J (2010) Flora of the Furka. Bauhinia 22:33–59

    Google Scholar 

  • Hobbie EA, Macko SA, Shugart HH (1999a) Insights into nitrogen and carbon dynamics of ectomycorrhizal and saprotrophic fungi from isotopic evidence. Oecologia 118:353–360

    Article  Google Scholar 

  • Hobbie EA, Macko SA, Shugart HH (1999b) Interpretation of nitrogen isotope signatures using the NIFTE model. Oecologia 120:405–415

    Article  Google Scholar 

  • Hobbie EA, Macko SA, Williams M (2000) Correlations between foliar delta N-15 and nitrogen concentrations may indicate plant-mycorrhizal interactions. Oecologia 122:273–283

    Article  Google Scholar 

  • Hobbie EA, Johnson MG, Rygiewicz PT, Tingey DT, Olszyk DM (2004) Isotopic estimates of new carbon inputs into litter and soils in a four-year climate change experiment with Douglas-fir. Plant Soil 259:331–343

    Article  CAS  Google Scholar 

  • Högberg P (1997)15 N natural abundance in soil-plant systems. New Phytol 137:179–203

    Article  Google Scholar 

  • Inauen N, Körner C, Hiltbrunner E (2012) No growth stimulation by CO2 enrichment in alpine glacier forefield plants. Glob Change Biol 18:985–999

    Article  Google Scholar 

  • Inauen N, Körner K, Hiltbrunner E (2013) Hydrological consequences of declining land use and elevated CO2 in alpine grassland. J Ecol 101:86–96

    Article  CAS  Google Scholar 

  • Ingestad T (1973) Mineral nutrient requirements of Vaccinium vitis-idaea and Vaccinium vitis-myrtillus. Physiol Plant 29:239–246

    Article  CAS  Google Scholar 

  • Jacot KA, Lüscher A, Suter M, Nosberger J, Hartwig UA (2005) Significance of legumes for the distribution of plant species in grassland ecosystems at different altitudes in the Alps. Plant Ecol 180:1–12

    Article  Google Scholar 

  • Kahmen A, Wanek W, Buchmann N (2008) Foliar delta15 N values characterize soil N cycling and reflect nitrate or ammonium preference of plants along a temperate grassland gradient. Oecologia 156:861–870

    Article  PubMed  PubMed Central  Google Scholar 

  • Kielland K (1994) Amino-acid absorption by arctic plants – implications for plant nutrition and nitrogen cycling. Ecology 75:2373–2383

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Körner C (2003) Alpine Plant Life. Springer, Berlin

    Book  Google Scholar 

  • Körner C (2007) The use of “altitude” in ecological research. Trends Ecol Evol 22:569–574

    Article  PubMed  Google Scholar 

  • Körner C, Diemer M (1987) In situ photosynthetic responses to light, temperature and carbon dioxide in herbaceous plants from low and high altitude. Funct Ecol 1:179–194

    Article  Google Scholar 

  • Körner C, Larcher W (1988) Plant life in cold climates. In: Long SF, Woodward FI (eds) Plants and temperature. Symp Soc Exp Biol 42:25–57, The Company of Biol Ltd, Cambridge

  • Körner C, Farquhar GD, Roksandic Z (1988) A global survey of carbon isotope discrimination in plants from high altitudes. Oecologia 74:623–632

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Körner C, Diemer M, Schäppi B, Niklaus P, Arnone J (1997) The responses of alpine grassland to four seasons of CO2 enrichment: a synthesis. Acta Oecol 18:165–175

    Article  Google Scholar 

  • Landolt E (1977) Ökologische Zeigerwerte zur Schweizer Flora. Veröff Geobot Inst ETH Zürich 64:1–208

    Google Scholar 

  • Landolt E, Bäumler B, Erhardt A, Hegg O, Klötzli F, Lämmler W, Nobis M, Rudmann-Maurer K, Schweingruber FH, Theurillat JP, Urmi E, Vust M, Wohlgemuth T (2010) Flora indicativa. Haupt, Bern

    Google Scholar 

  • Lesica P, Antibus RK (1986) Mycorrhizae of alpine fell-field communities on soils derived from crystalline and calcareous parent materials. Can J Bot 64:1691–1697

    Article  CAS  Google Scholar 

  • Mariotti A, Mariotti F, Amarger N, Pizelle G, Ngambi JM, Champigny ML, Moyse A (1980) Nitrogen isotope fractionation during nitrate absorption and atmospheric nitrogen-fixation by plants. Physiol Veg 18:163–181

    CAS  Google Scholar 

  • McDowell NG, Allen CD, Marshall L (2010) Growth, carbon-isotope discrimination, and drought-associated mortality across a Pinus ponderosa elevational transect. 16: 399–415

  • Michelsen A, Schmidt IK, Jonasson S, Quarmby C, Sleep D (1996) Leaf N-15 abundance of subarctic plants provides field evidence that ericoid, ectomycorrhizal and non- and arbuscular mycorrhizal species access different sources of soil nitrogen. Oecologia 105:53–63

    Article  Google Scholar 

  • Michelsen A, Quarmby C, Sleep D, Jonasson S (1998) Vascular plant N-15 natural abundance in heath and forest tundra ecosystems is closely correlated with presence and type of mycorrhizal fungi in roots. Oecologia 115:406–418

    Article  Google Scholar 

  • Mildner M, Bader M, Leuzinger S, Siegwolf R, Körner C (2014) Long-term 13C labeling provides evidence for temporal and special carbon allocation patterns in mature Picea abies. Oecologia 175:747–762

    Article  PubMed  Google Scholar 

  • Nadelhoffer KJ, Fry B (1994) Nitrogen isotope studies in forest ecosystems. In: Lajtha K, Michener R (eds) Stable isotopes in ecology. Blackwell, Oxford, pp 22–44

    Google Scholar 

  • Nadelhoffer K, Shaver G, Fry B, Giblin A, Johnson L, McKane R (1996) 15N natural abundances and N use by tundra plants. Oecologia 107:386–394

    Article  Google Scholar 

  • Nasholm T, Edfast AB, Ericsson A, Norden LG (1994) Accumulation of amino-acids in some boreal forest plants in response to increased nitrogen availability. New Phytol 126:137–143

    Article  Google Scholar 

  • O’Leary MH, Osmond CB (1980) Diffusional contribution to carbon isotope fractionation during dark CO2 fixation in CAM plants. Plant Physiol 66:931–934

    Article  PubMed  PubMed Central  Google Scholar 

  • Pardo LH, Templer PH, Goodale CL, Spoelstra J, Wessel W (2006) Regional assessment of N saturation using foliar and root δ15N. Biogeochem 80:143–171

    Article  Google Scholar 

  • Pate JS, Stewart GR, Unkovich M (1993) N15 natural abundance of plant and soil components of a Banksia woodland ecosystem in relation to nitrate utilization, life form, mycorrhizal status and N2-fixing abilities of component species. Plant Cell Env 16:365–373

    Article  CAS  Google Scholar 

  • Read DJ (1993) Plant-microbe mutualisms and community structure. Biodiv Ecosys Funct 99:181–209

    Google Scholar 

  • Robinson D (2001) δ15N as an integrator of the nitrogen cycle. Trends Ecol Evol 16:153–162

    Article  PubMed  Google Scholar 

  • Rorison IH (1985) Nitrogen source and the tolerance of Deschampsia flexuosa, Holcus lanatus and Bromus erectus to aluminium during seedling growth. J Ecol 73:83–90

    Article  CAS  Google Scholar 

  • Schulze E-D, Schimel DSS (2001) Uncertainties of global biogeochemical predictions. In: Schimel DS, Schulze E-D, Prentice IC, Heiman M, Harrison S, Holland E, Lloyd J (eds) Global biogeochemical cycles in the climate system. Academic Press, San Diego p, pp 3–14

    Chapter  Google Scholar 

  • Schulze ED, Chapini FSI, Gebauer G (1994) Nitrogen nutrition and isotope differences among life forms at the northern treeline of Alaska. Oecologia 100:406–412

    Article  Google Scholar 

  • Schulze ED, Williams RJ, Farquhar GD, Schulze W, Langridge J, Miller JM, Walker BH (1998) Carbon and nitrogen isotope discrimination and nitrogen nutrition of trees along a rainfall gradient in northern Australia. Aust J Plant Physiol 25:413–425

    Article  Google Scholar 

  • Seibt U, Abazar R, Griffiths H, Berry JA (2008) Carbon isotopes and water use efficiency: sense and sensitivity. Oecologia 155:441–454

    Article  PubMed  Google Scholar 

  • Shaver GR, Billings WD (1975) Root production and root turnover in a wet tundra ecosystem, Barrow, Alaska. Ecology 56:401–409

    Article  Google Scholar 

  • Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Rice Res Newsletter 15:14–15

    Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic Press, London

    Google Scholar 

  • Song MH, Duan DY, Chen H, Hu QW, Zhang F, Xu XL, Tian YQ, Ouyang H, Peng CH (2008) Leaf δ13C reflects ecosystem patterns and responses of alpine plants to the environments on the Tibetan Plateau. Ecography 31:499–508

    Article  Google Scholar 

  • Tcherkez G, Mahe A, Hodges M (2011) 12C/13C fractionations in plant primary metabolism. Trends Plant Sci 16:499–506

    CAS  PubMed  Google Scholar 

  • Thomas BD, Bowman WD (1998) Influence of N2-fixing Trifolium on plant species composition and biomass production in alpine tundra. Oecologia 115:26–31

    Article  Google Scholar 

  • Tomm GO, Van Kessel C, Slinkard AE (1994) Bi-directional transfer of nitrogen between alfalfa and bromegrass: short and long term evidence. Plant Soil 164:77–86

    Article  CAS  Google Scholar 

  • Von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of Phaseolus vulgaris cultivar Hawkesbury-Wonder leaves. Planta 153:376–387

    Article  Google Scholar 

  • Welker JM, Jonsdottir IS, Fahnestock JT (2003) Leaf isotopic (δ13C and δ15N) and nitrogen contents of Carex plants along the Eurasian Coastal Arctic: results from the Northeast Passage expedition. Polar Biol 27:29–37

    Article  Google Scholar 

  • Wielcke W, Krauss M, Amelung W (2002) Carbon isotope signature of polycyclic aromatic hydrocarbons (PAHs): evidence of different sources in tropical and temperate environments? Environ Sci Techn 36:3530–3535

    Article  Google Scholar 

  • Xu G, Huang TF, Zhang TF, Duan BL (2013) Significance of mesophyll conductance for photosynthetic capacity and water-use efficiency in response to alkaline stress in Populus cathayana seedlings. Photosynthetica 51:438–444

    Article  CAS  Google Scholar 

  • Yang Y, Siegwolf RTW, Körner C (2015) Species specific and environment induced variation of δ13C and δ15N in alpine plants. Frontiers Plant Sci. doi:10.3389/fpls.2015.00423

    Google Scholar 

  • Zhu Y, Siegwolf RTW, Durka W, Körner C (2010) Phylogenetically balanced evidence for structural and carbon isotope responses in plants along elevational gradients. Oecologia 162:853–863

    Article  PubMed  Google Scholar 

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Acknowledgments

We thank Catharina Lötscher and Mathias Saurer from the PSI in Villigen for their help with mass spectrometry analyses and Florian Schreier who helped with data analysis.

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Correspondence to Christian Körner.

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Körner, C., Leuzinger, S., Riedl, S. et al. Carbon and nitrogen stable isotope signals for an entire alpine flora, based on herbarium samples. Alp Botany 126, 153–166 (2016). https://doi.org/10.1007/s00035-016-0170-x

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