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Higher capability of C3 than C4 plants to use nitrogen inferred from nitrogen stable isotopes along an aridity gradient

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Abstract

Background and aims

The nitrogen isotope composition (δ15N) of plants in arid and semiarid grasslands is affected by environmental factors, especially water availability. Nevertheless, it is unclear whether the response of δ15N to water availability differs between C3 and C4 photosynthetic pathways.

Methods

We investigated plant δ15N of coexisting C3 and C4 species as a function of aridity along a 3200 km aridity gradient across the arid and semi-arid grasslands of northern China.

Results

Aridity was positively correlated with plant δ15N values in both C3 and C4 plants and also in the entire plant community, whereas soil bulk δ15N values increased first and then decreased along the aridity gradient. The N uptake by C4 plants appeared to be more affected by competition pressure of neighboring plants and soil microbes than for C3 plants along the transect.

Conclusions

The decoupled relationship between plant and soil δ15N values indicated that variations in vegetation and soil δ15N values were driven by differential biogeochemical processes, while different soil N sources were used for plant growth along the climatic gradient. The advantage of C3 plants in the use of N may counteract the competitive advantage that C4 plants have over C3 plants due to their higher water use efficiency under drier conditions. These findings can help understand why C4 plants do not completely replace C3 plants in drier environments despite their higher water use efficiency.

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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. Glob Biogeochem Cycles 17:1031. https://doi.org/10.1029/2002GB001903

    Article  CAS  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 Chang Biol 10:359–373

    Article  Google Scholar 

  • Aranibar JN, Anderson IC, Epstein HE, Feral CJW, Swap RJ, Ramontsho J, Macko SA (2008) Nitrogen isotope composition of soils, C3 and C4 plants along land use gradients in southern Africa. J Arid Environ 72:326–337

    Article  Google Scholar 

  • Austin AT, Sala OE (1999) Foliar δ15N is negatively correlated with rainfall along the IGBP transect in Australia. Aust J Plant Physiol 26:293–295

    Article  Google Scholar 

  • Bai Y, Han X, Wu J, Chen Z, Li L (2004) Ecosystem stability and compensatory effects in the Inner Mongolia grassland. Nature 431:181–184

    Article  PubMed  CAS  Google Scholar 

  • Brown R (1978) A difference in N use efficiency in C3 and C4 plants and its implications in adaptation and evolution. Crop Sci 18:93–98

    Article  CAS  Google Scholar 

  • Cai J, Weiner J, Wang R, Luo W, Zhang Y, Liu H, Xu Z, Li H, Zhang Y, Jiang Y (2017) Effects of nitrogen and water addition on trace element stoichiometry in five grassland species. J Plant Res 130(4):659–668

    Article  PubMed  CAS  Google Scholar 

  • Cerling TE, Harris JM, MacFadden BJ, Leakey MG, Quade J, Eisenmann V, Ehleringer JR (1997) Global vegetation change through the Miocene/Pliocene boundary. Nature 389:153–158

    Article  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Craine JM, Brookshire ENJ, Cramer MD, Hasselquist NJ, Koba K, Marin-Spiotta E, Wang L (2015) Ecological interpretations of nitrogen isotope ratios of terrestrial plants and soils. Plant Soil 396:1–26

    Article  CAS  Google Scholar 

  • Cramer MD, Hawkins HJ, Verboom GA (2009) The importance of nutritional regulation of plant water flux. Oecologia 161:15–24

    Article  PubMed  Google Scholar 

  • Dalal RC, Strong WM, Cooper JE, King AJ (2013) Relationship between water use and nitrogen use efficiency discerned by 13C discrimination and 15N isotope ratio in bread wheat grown under no-till. Soil Tillage Res 128:110–118

    Article  Google Scholar 

  • Díaz FP, Frugone M, Gutiérrez RA, Latorre C (2016) Nitrogen cycling in an extreme hyperarid environment inferred from δ15N analyses of plants, soils and herbivore diet. Sci Rep 6:22226. https://doi.org/10.1038/srep22226

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dijkstra FA, Carrillo Y, Aspinwall MJ, Maier C, Canarini A, Tahaei H, Choat B, Tissue DT (2016) Water, nitrogen and phosphorus use efficiencies of four tree species in response to variable water and nutrient supply. Plant Soil 406:187–199

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  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

    Article  Google Scholar 

  • Harrison KA, Bol R, Bardgett RD (2007) Preferences for different nitrogen forms by coexisting plant species and soil microbes. Ecology 88:989–999

    Article  PubMed  Google Scholar 

  • Hartman G, Danin A (2010) Isotopic values of plants in relation to water availability in the eastern Mediterranean region. Oecologia 162:837–852

    Article  PubMed  Google Scholar 

  • Heaton TH (1987) The 15N/14N ratios of plants in South Africa and Namibia: relationship to climate and coastal/saline environments. Oecologia 74:236–246

    Article  PubMed  CAS  Google Scholar 

  • Hilbig W (1995) The vegetation of Mongolia. SPB Academic Publishing, Amsterdam

  • Hobbie EA, Colpaert JV (2003) Nitrogen availability and colonization by mycorrhizal fungi correlate with nitrogen isotope patterns in plants. New Phytol 157:115–126

    Article  CAS  Google Scholar 

  • Hobbie EA, Högberg P (2012) Nitrogen isotopes link mycorrhizal fungi and plants to nitrogen dynamics. New Phytol 196:367–382

    Article  PubMed  CAS  Google Scholar 

  • Hobbie EA, Ouimette AP (2009) Controls of nitrogen isotope patterns in soil profiles. Biogeochemistry 95:355–371

    Article  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Houlton BZ, Sigman DM, Schuur EA, Hedin LO (2007) A climate-driven switch in plant nitrogen acquisition within tropical forest communities. Proc Natl Acad Sci USA 104:8902–8906

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kahmen A, Wanek W, Buchmann N (2008) Foliar δ15N 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 

  • Kichenin E, Wardle DA, Peltzer DA, Morse CW, Freschet GT (2013) Contrasting effects of plant inter- and intraspecific variation on community-level trait measures along an environmental gradient. Funct Ecol 27:1254–1261

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Liu Q, Qiao N, Xu X, Xin X, Han JY, Tian Y, Ouyang H, Kuzyakov Y (2016) Nitrogen acquisition by plants and microorganisms in a temperate grassland. Sci Rep 6:22642. https://doi.org/10.1038/srep22642

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu D, Zhu W, Wang X, Pan Y, Wang C, Xi D, Bai E, Wang Y, Han X, Fang Y (2017) Abiotic versus biotic controls on soil nitrogen cycling in drylands along a 3200km transect. Biogeosciences 14:989–1001

    Article  CAS  Google Scholar 

  • Luo W, Elser JJ, Lü XT, Wang Z, Bai E, Yan C, Wang C, Li MH, Zimmermann NE, Han X (2015) Plant nutrients do not covary with soil nutrients under changing climatic conditions. Glob Biogeochem Cycles 29:1298–1308

    Article  CAS  Google Scholar 

  • Luo W, Sardans J, Dijkstra FA, Peñuelas J, Lü XT, Wu H, Li MH, Bai E, Wang Z, Han X, Jiang Y (2016) Thresholds in decoupled soil-plant elements under changing climatic conditions. Plant Soil 409:159–173

    Article  CAS  Google Scholar 

  • Mariotte P, Vandenberghe C, Kardol P, Hagedorn F, Buttler A (2013) Subordinate plant species enhance community resistance against drought in semi-natural grasslands. J Ecol 101:763–773

    Article  Google Scholar 

  • McCulley RL, Burke IC, Lauenroth WK (2009) Conservation of nitrogen increases with precipitation across a major grassland gradient in the central Great Plains of North America. Oecologia 159:571–581

    Article  PubMed  Google Scholar 

  • Michelsen A, Quarmby C, Sleep D, Jonasson S (1998) Vascular plant 15N 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  PubMed  Google Scholar 

  • Murphy BP, Bowman D (2009) The carbon and nitrogen isotope composition of Australian grasses in relation to climate. Funct Ecol 23:1040–1049

    Article  Google Scholar 

  • Ni J (2003) Plant functional types and climate along a precipitation gradient in temperate grasslands, north-east China and south-east Mongolia. J Arid Environ 53:501–516

    Article  Google Scholar 

  • Ogaya R, Peñuelas J (2008) Changes in leaf δ13C and δ15N for three Mediterranean tree species in relation to soil water availability. Acta Oecol 34:331–338

    Article  Google Scholar 

  • Ouyang S, Tian Y, Liu Q, Zhang L, Wang R, Xu X (2016) Nitrogen competition between three dominant plant species and microbes in a temperate grassland. Plant Soil 408:121–132

    Article  CAS  Google Scholar 

  • Pardo L, Templer P, Goodale C, Duke S, Groffman P, Adams M, Boeckx P, Boggs J, Campbell J, Colman B (2006) Regional assessment of N saturation using foliar and root δ15N. Biogeochemistry 80:143–171

    Article  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. Glob Chang Biol 18:311–321

    Article  Google Scholar 

  • Pyankov VI, Gunin PD, Tsoog S, Black CC (2000) C4 plants in the vegetation of Mongolia: their natural occurrence and geographical distribution in relation to climate. Oecologia 123:15–31

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Sage RF, Pearcy RW (1987a) The nitrogen use efficiency of C3 and C4 plants I. Leaf nitrogen, growth, and biomass partitioning in Chenopodium album (L.) and Amaranthus retroflexus (L.). Plant Physiol 84:954–958

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sage RF, Pearcy RW (1987b) The nitrogen use efficiency of C3 and C4 plants II. Leaf nitrogen effects on the gas exchange characteristics of Chenopodium album (L.) and Amaranthus retroflexus (L.). Plant Physiol 84:959–963

    Article  PubMed  PubMed Central  CAS  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 

  • Swap RJ, Aranibar JN, Dowty PR, Gilhooly WP, Macko SA (2004) Natural abundance of 13C and 15N in C3 and C4 vegetation of southern Africa: patterns and implications. Glob Chang Biol 10:350–358

    Article  Google Scholar 

  • Takebayashi Y, Koba K, Sasaki Y, Fang Y, Yoh M (2010) The natural abundance of 15N in plant and soil-available N indicates a shift of main plant N resources to NO3 − from NH4 + along the N leaching gradient. Rapid Commun Mass Spectrom 24:1001–1008

    Article  PubMed  CAS  Google Scholar 

  • Wang C, Wang X, Liu D, Wu H, Lu X, Fang Y, Cheng W, Luo W, Jiang P, Shi J, Yin H, Zhou J, Han X, Bai E (2014) Aridity threshold in controlling ecosystem nitrogen cycling in arid and semi-arid grasslands. Nat Commun 5:499. https://doi.org/10.1038/ncomms5799

    Article  CAS  Google Scholar 

  • Wang R, Tian Y, Ouyang S, Xu X, Xu F, Zhang Y (2016) Nitrogen acquisition strategies used by Leymus chinensis and Stipa grandis in temperate steppes. Biol Fertil Soils 52:951–961

    Article  CAS  Google Scholar 

  • Watson L, Dallwitz MJ (1992) Grass genera of the world: descriptions, illustrations, identification, and information retrieval; including synonyms, morphology, anatomy, physiology, phytochemistry, cytology, classification, pathogens, world and local distribution, and references. http://delta-intkey.com/grass/www/index.htm

  • Wittmer MH, Auerswald K, Bai Y, Schaeufele R, Schnyder H (2010) Changes in the abundance of C3/C4 species of Inner Mongolia grassland: evidence from isotopic composition of soil and vegetation. Glob Chang Biol 16:605–616

    Article  Google Scholar 

  • Wooller MJ, Johnson BJ, Wilkie A, Fogel ML (2005) Stable isotope characteristics across narrow savanna/woodland ecotones in Wolfe Creek meteorite crater, Western Australia. Oecologia 145:100–112

    Article  PubMed  Google Scholar 

  • Xue D, Botte J, De Baets B, Accoe F, Nestler A, Taylor P, Van Cleemput O, Berglund M, Boeckx P (2009) Present limitations and future prospects of stable isotope methods for nitrate source identification in surface-and groundwater. Water Res 43:1159–1170

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We thank all members of the Field Expedition Team from the Institute of Applied Ecology, Chinese Academy of Sciences, for assistance with the collection of the field data. We thank three anonymous referees as well as the Handling Editor for constructive comments on the manuscript. This work was supported by the National Basic Research Program of China (2016YFC0500601, 2016YFC0500700 and 2015CB150802), National Natural Science Foundation of China (41600302, 3231470505 and 41273094), Strategic Priority Research Program of the Chinese Academy of Sciences (XDB15010403), Youth Innovation Promotion Association CAS (2014174), and the Key Research Program from CAS (KFZD-SW-305-002). JP and JS were funded by the European Research Council Synergy grant ERC-SyG-2013-610028, IMBALANCE-P, the Spanish Government grant CGL2013-48074-P and the Catalan Government grant SGR 2014-274.

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Authors and Affiliations

  1. Erguna Forest-Steppe Ecotone Research Station, Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang, 110164, China

    Wentao Luo, Xiaoguang Wang, Zhengwen Wang, Xiao-Tao Lü & Xingguo Han

  2. College of Environment and Resources, Dalian Minzu University, Dalian, 116600, China

    Xiaoguang Wang

  3. CSIC, Global Ecology Unit CREAF-CSIC-UAB, 08193, Bellaterra, Catalonia, Spain

    Jordi Sardans & Josep Peñuelas

  4. CREAF, 08193, Cerdanyola del Vallès, Catalonia, Spain

    Jordi Sardans & Josep Peñuelas

  5. Sydney Institute of Agriculture, School of Life and Environmental Sciences, The University of Sydney, Sydney, NSW, 2006, Australia

    Feike A. Dijkstra

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  1. Wentao Luo
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  2. Xiaoguang Wang
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Correspondence to Xiao-Tao Lü.

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Luo, W., Wang, X., Sardans, J. et al. Higher capability of C3 than C4 plants to use nitrogen inferred from nitrogen stable isotopes along an aridity gradient. Plant Soil 428, 93–103 (2018). https://doi.org/10.1007/s11104-018-3661-2

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