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Patterns of foliar and soil nitrogen isotope composition of Caragana microphylla, a leguminous shrub species in the semi-arid regions of northern China

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Abstract

Variation in foliar and soil nitrogen (N) isotope composition (δ15N) across environmental gradients has been widely studied at various scales. However, much less is known about the patterns of N2-fixing species that are presumed to be independent of climatic factors due to their capacity to fix atmospheric N2. In this study, the foliar and soil δ15N in Caragana microphylla, a leguminous shrub important for its role in controlling soil erosion and land desertification in northern China, were determined from 23 sites along an east–west transect across the species distribution range. The soil δ15N tended to be significantly higher than the foliar δ15N and there was a positive correlation between them (r2 = 0.58, p < 0.0001), though substantial variability was found in foliar and soil δ15N across all sites. Both soil and foliar δ15N were negatively correlated with precipitation, temperature, dry N deposition (DND) and longitude, but positively correlated with foliar N, soil N and altitude. The structural equation modeling further suggested growing season precipitation indirectly influenced foliar δ15N by its direct impact on soil δ15N and by its indirect impact on soil δ15N via DND and total N deposition (TND), whereas growing season temperature affected foliar δ15N indirectly both by its effect on foliar N and by its effect on soil δ15N via WND, TND and foliar N. Altogether, our results indicated that foliar δ15N also shifted along environmental gradients in leguminous plant species and showed primary dependence on soil δ15N, confirming previous findings in non-leguminous plants. These results augment our common understanding of foliar and soil δ15N patterns across climatic gradients in plants.

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References

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

    Google Scholar 

  • Aranibar JN, Otter L, Macko SA, Feral CJW, Epstein HE, Dowty PR, Eckardt F, Shugart HH, Swap RJ (2004) Nitrogen cycling in the soil-plant system along a precipitation gradient in the Kalahari sands. Glob Change Biol 10:359–373

    Google Scholar 

  • Averill C, Finzi A (2011) Increasing plant use of organic nitrogen with elevation is reflected in nitrogen uptake rates and ecosystem δ15N. Ecology 92:883–891

    Google Scholar 

  • Chen LT, Flynn DF, Zhang XW, Gao XL, Lin L, Luo J, Zhao CM (2015) Divergent patterns of foliar δ13C and δ15N in Quercus aquifolioides with an altitudinal transect on the Tibetan Plateau: an integrated study based on multiple key leaf functional traits. J Plant Ecol 8:303–312

    Google Scholar 

  • Cheng WX, Chen QS, Xu YQ, Han XG, Li LH (2009) Climate and ecosystem 15N natural abundance along a transect of Inner Mongolian grasslands: contrasting regional patterns and global patterns. Glob Biogeochem Cycle 23:1–11

    Google Scholar 

  • Cheng SL, Fang HJ, Yu GR, Zhu TH, Zheng JJ (2010) Foliar and soil 15N natural abundances provide field evidence on nitrogen dynamics in temperate and boreal forest ecosystems. Plant Soil 337:285–297

    Google Scholar 

  • Craine JM, Lee WG, Bond WJ, Williams RJ, Johnson LC (2005) Environmental constraints on a global relationship among leaf and root traits of grasses. Ecology 86:12–19

    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, Peñuelas 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

    Google Scholar 

  • Craine JM, Towne EG, Ocheltree TW, Nippert JB (2012) Community traitscape of foliar nitrogen isotopes reveals N availability patterns in a tallgrass prairie. Plant Soil 356:395–403

    Google Scholar 

  • Craine JM, Elmore AJ, Wang L, Augusto L, Baisden WT, Brookshire ENJ, Cramer MD, Hasselquist NJ, Hobbie EA, Kahmen A, Koba K, Kranabetter JM, Mack MC, MarinSpiotta E, Mayor JR, McLauchlan KK, Michelsen A, Nardoto GB, Oliveira RS, Perakis SS, Peri PL, Quesada CA, Richter A, Schipper LA, Stevenson BA, Turner BL, Viani RAG, Wanek W, Zeller B (2015) Convergence of soil nitrogen isotopes across global climate gradients. Sci Rep 5:8280

    Google Scholar 

  • Craine JM, Elmore AJ, Wang LX, Aranibar J, Bauters M, Boeckx P, Crowley BE, Dawes MA, Delzon S, Fajardo A, Fang YT, Fujiyoshi L, Gray A, Guerrieri R, Gundale MJ, Hawke DJ, Hietz P, Jonard M, Kearsley E, Kenzo T, Makarov M, Marañón-Jiménez S, McGlynn TP, McNeil BE, Mosher SG, Nelson DM, Peri PL, Roggy JC, Sanders-DeMott R, Song MH, Szpak P, Templer PH, Van der Colff D, Werner C, Xu XL, Yang Y, Yu GR, Zmudczyńska-Skarbek K (2018) Isotopic evidence for oligotrophication of terrestrial ecosystems. Nat Ecol Evol 2:1735–1744

    Google Scholar 

  • Dawson TE, Mambelli S, Plamboeck AH, Templer PH, Tu KP (2002) Stable isotopes in plant ecology. Annu Rev Ecol Syst 33:507–559

    Google Scholar 

  • Evans RD (2001) Physiological mechanisms influencing plant nitrogen isotope composition. Trends Plant Sci 6:121–126

    Google Scholar 

  • Freitas ADSD, Ramos APDS, Lyra RP, Araújo EL (2015) Nitrogen isotopic patterns in tropical forests along a rainfall gradient in northeast Brazil. Plant Soil 391:109–122

    Google Scholar 

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

    Google Scholar 

  • Han W, Fang J, Guo D, Zhang Y (2005) Leaf nitrogen and phosphorus stoichiometry across 753 terrestrial plant species in China. New Phytol 168:377–385

    Google Scholar 

  • Handley LL, Austin AT, Robinson D, Scrimgeour CM, Raven JA, Heaton THE, Schmidt S, Stewart GR (1999) The 15N natural abundance (δ15N) of ecosystem samples reflects measures of water availability. Aust J Plant Physiol 26:185–199

    Google Scholar 

  • Hobbie EA, Macko SA, Williams M (2000) Correlations between foliar δ15N and nitrogen concentrations may indicate plant-mycorrhizal interactions. Oecologia 122:273–283

    Google Scholar 

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

    Google Scholar 

  • Houlton B, Sigman D, Hedin L (2006) Isotopic evidence for large gaseous nitrogen losses from tropical rainforests. Proc Natl Acad Sci USA 103:8745–8750

    Google Scholar 

  • IPCC (2013) Climate change 2013: the physical science basis. Cambridge University Press, Cambridge

    Google Scholar 

  • Knapp AK, Beier C, Briske DD, Classen AT, Luo YQ, Reichstein M, Smith MD, Bell JE, Fay PA, Heisler JL, Leavitt SW, Sherry R, Smith B, Weng E (2008) Consequences of more extreme precipitation regimes for terrestrial ecosystems. Bioscience 58:811–821

    Google Scholar 

  • Kolb KJ, Evans RD (2002) Implications of leaf nitrogen recycling on the nitrogen isotope composition of deciduous plant tissues. New Phytol 156:57–64

    Google Scholar 

  • Kozlowski TT, Pallardy SG (2002) Acclimation and adaptive responses of woody plants to environmental stresses. Bot Rev 68:270–334

    Google Scholar 

  • Liu WG, Wang Z (2009) Nitrogen isotopic composition of plant-soil in the Loess Plateau and its responding to environmental change. Chinese Sci Bull 54:272–279

    Google Scholar 

  • Liu X, Wang G, Li J, Wang Q (2010) Nitrogen isotope composition characteristics of modern plants and their variations along an altitudinal gradient in Dongling Mountain in Beijing. Sci China Earth Sci 53:128–140

    Google Scholar 

  • Ma CC, Gao YB, Guo HY, Wang JL, Wu JB, Xu JS (2008) Physiological adaptations of four dominant Caragana species in the desert region of the Inner Mongolia Plateau. J Arid Environ 72:247–254

    Google Scholar 

  • Ma F, Na XF, Xu TT (2016) Drought responses of three closely related Caragana species: implication for their vicarious distribution. Ecol Evol 6:2763–2773

    Google Scholar 

  • Ma F, Xu TT, Li M, Liu JL, Sun ZJ (2018) Precipitation is the main factor affecting the variation of foliar nitrogen isotope composition in two leguminous shrub species of northwestern China. Biol Lett 14:20180382

    Google Scholar 

  • Martinelli LA, Piccolo MC, Townsend AR, Vitousek PM, Cuevas E, McDowell W, Robertson GP, Santos OC, Treseder K (1999) Nitrogen stable isotope composition of leaves and soil: tropical versus temperate forests. Biogeochemistry 46:45–65

    Google Scholar 

  • Miao SY, Long LD, Tao WQ, Zeng QC, Chen JH, Huang JL, Wu QH, Tang YJ (2016) Composition of stable carbon and nitrogen isotopes in five wetland plants and sediments from the Pearl River estuary, South China. Chem Ecol 32:1–15

    Google Scholar 

  • Na XF, Xu TT, Li M, Ma F, Kardol P (2017) Bacterial diversity in the rhizosphere of two phylogenetically closely related plant species across environmental gradients. J Soil Sediment 17:1–11

    Google Scholar 

  • Pardo LH, Templer PH, Goodale CL, Duke S, Groffman PM, Adams MB, Boeckx P, Boggs J, Campbell J, Colman B, Compton J, Emmett B, Gundersen P, Kjønaas J, Lovett G, Mack M, Magill A, Mbila M, Mitchell MJ, McGee G, McNulty S, Nadelhoffer K, Ollinger S, Ross D, Rueth H, Rustad L, Schaberg P, Schiff S, Schleppi P, Spoelstra J, Wessel W (2006) Regional assessment of N saturation using foliar and root δ15N. Biogeochemistry 80:143–171

    Google Scholar 

  • Peri PL, Ladd B, Pepper DA, Bonser SP, Laffan SW, Amelung W (2012) Carbon (δ13C) and nitrogen (δ15N) stable isotope composition in plant and soil in Southern Patagonia’s native forests. Global Change Biol 18:311–321

    Google Scholar 

  • Reich PB, Oleksyn J (2004) Global patterns of plant leaf N and P in relation to temperature and latitude. Proc Natl Acad Sci 101:11001–11006

    Google Scholar 

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

    Google Scholar 

  • Sah S, Brumme R (2003) Altitudinal gradients of natural abundance of stable isotopes of nitrogen and carbon in the needles and soil of a pine forest in Nepal. J For Sci 49:19–26

    Google Scholar 

  • Sah SP, Rita H, Ilvesniemi H (2006) 15N natural abundance of foliage and soil across boreal forests of Finland. Biogeochemistry 80:277–288

    Google Scholar 

  • Schmidt S, Stewart G (2003) δ15N values of tropical savanna and monsoon forest species reflect root specialisations and soil nitrogen status. Oecologia 134:569–577

    Google Scholar 

  • Schulze ED, Nicolle D, Boerner A, Lauerer M, Aas G, Schulze I (2014) Stable carbon and nitrogen isotope ratios of Eucalyptus, and Acacia, species along a seasonal rainfall gradient in western Australia. Trees 28:1125–1135

    Google Scholar 

  • Virginia RA, Delwiche CC (1982) Natural 15N abundance of presumed N2-fxing and non-N2-fxing plants from selected ecosystems. Oecologia 54:317–325

    Google Scholar 

  • Vitousek PM, Shearer G, Kohl DH (1989) Foliar 15N natural abundance in Hawaiian rainforest: patterns and possible mechanisms. Oecologia 78:383–388

    Google Scholar 

  • Wang C, Wang XB, Liu DW, Wu HH, Lü XT, Fang YT, Cheng WX, Luo WT, Jiang P, Shi J, Yin HG, Zhou JZ, Han XG, Bai E (2014) Aridity threshold in controlling ecosystem nitrogen cycling in arid and semi-arid grasslands. Nat Commun 5:4799

    Google Scholar 

  • Warren C, McGrath J, Adams M (2001) Water availability and carbon isotope discrimination in conifers. Oecologia 127:476–486

    Google Scholar 

  • Yang Y, Ji C, Robinson D, Zhu B, Fang H, Shen H, Fang J (2013) Vegetation and soil 15N natural abundance in alpine grasslands on the Tibetan Plateau: patterns and implications. Ecosystems 16:1013–1024

    Google Scholar 

  • Yang Y, Siegwolf RTW, Koerner C (2015) Species specific and environment induced variation of δ13C and δ15N in alpine plants. Front Plant Sci 6:423

    Google Scholar 

  • Yu G, Jia Y, He N, Zhu J, Chen Z, Wang Q, Piao S, Liu X, He H, Guo X, Wen Z, Li P, Ding G, Goulding K (2019) Stabilization of atmospheric nitrogen deposition in China over the past decade. Nat Geosci 12:424–429

    Google Scholar 

  • Zhang ML, Fritsch PW, Cruz BC (2009) Phylogeny of Caragana (Fabaceae) based on DNA sequence data from rbcL, trnS–trnG, and ITS. Mol Phylogenet Evol 50:547–559

    Google Scholar 

  • Zhang H, Lü X, Knapp AK, Hartmann H, Bai E, Wang X, Yu Q, Han X (2018) Facilitation by leguminous shrubs increases along a precipitation gradient. Funct Ecol 32:203–213

    Google Scholar 

  • Zhou Y, Cheng X, Fan J, Harris W (2016) Patterns and controls of foliar nitrogen isotope composition on the Qinghai-Tibet plateau, China. Plant Soil 406:1–12

    Google Scholar 

  • Zhou Y, Li H, Cheng X, Xu X, Zhang H, Zhang W, Liu L, Li Y, Song C (2017) Patterns of soil and plant nitrogen isotope composition and their relationships with climate factors in Xilingol League, Inner Mongolia, China. Plant Ecol Divers 10:521–528

    Google Scholar 

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Acknowledgements

We thank the editor and the two anonymous reviewers for their constructive comments. This study was funded by the National Natural Science Foundation of China (Nos. 31860142, 31760056, 31260166).

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Authors and Affiliations

  1. Institute of Environmental Engineer, Ningxia University, Yinchuan, 750021, People’s Republic of China

    Fei Ma & GuoJu Xiao

  2. Key Laboratory of Forest Ecology and Management, Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang, 110016, People’s Republic of China

    Shanlong Li

  3. School of Life Science, Ningxia University, Yinchuan, 750021, People’s Republic of China

    Tingting Xu

  4. College of Resources and Environmental Science, Ningxia University, Yinchuan, 750021, People’s Republic of China

    Zhaona Zhou & Zhe Ai

  5. Forestry College, Hebei Agricultural University, Baoding, 071001, People’s Republic of China

    Yanlong Jia

  6. School of Agriculture, Food and Wine, The University of Adelaide South Australia, Adelaide, 5064, Australia

    Matthew D. Denton

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  1. Fei Ma
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Correspondence to Tingting Xu.

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Ma, F., Zhou, Z., Li, S. et al. Patterns of foliar and soil nitrogen isotope composition of Caragana microphylla, a leguminous shrub species in the semi-arid regions of northern China. Biogeochemistry 146, 257–269 (2019). https://doi.org/10.1007/s10533-019-00617-x

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