Skip to main content
SpringerLink
Log in

Short-term effects of soil warming and nitrogen addition on the N:P stoichiometry of Cunninghamia lanceolata in subtropical regions

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Aims

Increasing temperature and nitrogen (N) deposition are major drivers of global change that will influence plant-soil systems. We aimed to understand how plant stoichiometry and nutrient limiting types could change with continued warming and N inputs in subtropical regions.

Methods

In 2014, the experiments were established in 30 mini-plots (2 × 2 m) with the following treatments: control, high N addition, low N addition, warming, warming + high N addition, and warming + low N addition. We sampled the leaf and root of Cunninghamia lanceolata and soils to assess their elemental and stoichiometric variables and δ15N under all six conditions.

Results

Both experimental warming and N fertilization consistently induced an increase in fine-root N, P, and N:P. The N:P ratio of the mature green-leaf and soil was 7.24–11.63 and 4.79–6.56, respectively. On average, C. lanceolata showed higher proportional P resorption, but lower N resorption. The δ15N enrichment factor significantly increased in the warming and N addition treatments.

Conclusions

N addition decrease leaf N content, and increased the plant growth, which was due to the effect of the N dilution of C. lanceolata. In subtropical regions, N-limitation affects the growth of C. lanceolata, and the concurrent increase in warming and N fertilization should help relieve N-limiting conditions.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Aerts R (1996) Nutrient resorption from senescing leaves of perennials: are there general patterns? J Ecol 84:597–608

    Article  Google Scholar 

  • Amundson R, Amundson R (2004) New insights into the global patterns of the isotopic composition of soil and plant nitrogen. Glob Biogeochem Cycle 17:2076–2079

    Google Scholar 

  • Brant AN, Chen HYH (2015) Patterns and mechanisms of nutrient resorption in plants. Crit Rev Plant Sci 34:471–486

    Article  CAS  Google Scholar 

  • Camenzind T, Hempel S, Homeier J, Horn S, Velescu A, Wilcke W, Rillig MC (2014) Nitrogen and phosphorus additions impact arbuscular mycorrhizal abundance and molecular diversity in a tropical montane forest. Glob Chang Biol 20:3646–3659

    Article  PubMed  Google Scholar 

  • Carter M, Gregorich E, Adl S M, Acosta-Mercado D, Anderson, TR, Lynn DH, Carter M, Acosta-Mercado D, Anderson TR, Lynn DH (1993) Soil Sampling and Methods of Analysis (2nd edition). Mercado

  • Chen ZQ, Chen ZB, Yan XY, Bai LY (2016) Stoichiometric mechanisms of Dicranopteris dichotoma growth and resistance to nutrient limitation in the Zhuxi watershed in the red soil hilly region of China. Plant Soil 398:367–379

    Article  CAS  Google Scholar 

  • Chen FS, Niklas KJ, Chen GS, Guo D (2012) Leaf traits and relationships differ with season as well as among species groupings in a managed Southeastern China forest landscape. Plant Ecol 213:1489–1502

    Article  Google Scholar 

  • Chen FS, Niklas KJ, Liu Y, Fang XM, Wan SZ, Wang HM (2015) Nitrogen and phosphorus additions alter nutrient dynamics but not resorption efficiencies of Cunninghamia lanceolata leaves and twigs differing in age. Tree Physiol. doi:10.1093/treephys/tpv076

    PubMed Central  Google Scholar 

  • Cleveland CC, Townsend AR, Tayor P, Alvarez-Clare S, Bustamante Mercedes MC, George C, Dobrowski SZ, Grierson P, Harms KE, Houlton BZ, Marklein A, Parton W, Porder S, Reed SC, Sierra CA, Silver WL, Tanner EVJ, Wilder WR (2011) Relationships among net primary productivity, nutrients and climate in tropical rain forest: a pan-tropical analysis. Ecol Lett 14:1313–1317

    Article  Google Scholar 

  • Dijkstra FA, Pendall E, Morgan JA, Blumenthal DM, Carrillo Y, LeCain DR, Follett RF, Williams DG (2012) Climate change alters stoichiometry of phosphorus and nitrogen in a semiarid grassland. New Phytol 196:808–815

    Article  Google Scholar 

  • D’Orangeville L, Houle D, Côté B, Duchesne L (2014) Soil response to a 3-year increase in temperature and nitrogen deposition measured in a mature boreal forest using ion-exchange membranes. Environ Monit Assess 186:8191–8202

    Article  PubMed  Google Scholar 

  • Fan HB, Wu JP, Liu WF, Yuan YH, Hu L, Cai QK (2015) Linkages of plant and soil C: N: P stoichiometry and their relationships to forest growth in subtropical plantations. Plant Soil 392:127–138

    Article  CAS  Google Scholar 

  • Fröberg M, Grip H, Tipping E, Svensson M, Strömgren M, Dan B (2013) Long-term effects of experimental fertilization and soil warming on dissolved organic matter leaching from a spruce forest in Northern Sweden. Geoderma 200–201:172–179

    Article  Google Scholar 

  • Garten CT, Miegroet HV (1994) Relationships between soil nitrogen dynamics and natural 15N-abundance in plant foliage from the Great Smoky Mountains National Park. Can J For Res 24:1636–1645

    Article  Google Scholar 

  • Gundale MJ, From F, Bach LH, Nordin A (2014) Anthropogenic nitrogen deposition in boreal forests has a minor impact on the global carbon cycle. Glob Chang Biol 20:276–286

    Article  PubMed  Google Scholar 

  • Güsewell S (2004) N:P ratios in terrestrial plants: variation and functional significance. New Phytol 164:243–266

    Article  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(2):377–385

  • Handley LL, Austin AT, Stewart GR, Robinson D, Scrimgeour CM, Raven JA, Heaton THE, Schmidt S (1999) The 15N natural abundance (δ15N) of ecosystem samples reflects measures of water availability. Aust J Plant Physiol 26(2):186–199

  • Hayat R, Ahmed I, Sheirdil RA (2012) An overview of plant growth promoting rhizobacteria (PGPR) for sustainable agriculture. Crop Production for Agricultural Improvement: 557–579

  • Hodge A, Storer K (2015) Arbuscular mycorrhiza and nitrogen: implications for individual plants through to ecosystems. Plant Soil 386:1–19

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • IPCC (2013) Climate Change 2013: The Physical Science Basis. Working Group I: Contribution to the Intergovernmental Panel on Climate Change Fifth Assessment Report. Cambridge University Press, Cambridge

  • Kähkölä AK, Nygren P, Leblanc HA, Pennanen T, Pietikäinen J (2012) Leaf and root litter of a legume tree as nitrogen sources for cacaos with different root colonization by arbuscular mycorrhizae. Nutr Cycl Agroecosyst 92:51–65

    Article  Google Scholar 

  • Khan MH, Meghvansi MK, Gupta R, Veer V (2015) Elemental stoichiometry indicates predominant influence of potassium and phosphorous limitation on arbuscular mycorrhizal symbiosis in acidic soil at high altitude. J Plant Physiol 189:105–112

    Article  CAS  PubMed  Google Scholar 

  • Koerselman W, Meuleman AFM (1996) The vegetation N:P ratio: a new tool to detect the nature of nutrient limitation. J Appl Ecol 33:1441–1450

    Article  Google Scholar 

  • Koller EK, Press MC, Callaghan TV, Phoenix GK (2016) Tight coupling between shoot level foliar N and P, leaf area, and shoot growth in Arctic Dwarf Shrubs under simulated climate change. Ecosystems 19:326–338

    Article  CAS  Google Scholar 

  • Lebauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89:371–379

    Article  PubMed  Google Scholar 

  • Leppälammi-Kujansuu J, Ostonen I, Strömgren M, Nilsson LO, Kleja DB, Sah SP, Helmisaari HS (2013) Effects of long-term temperature and nutrient manipulation on Norway spruce fine roots and mycelia production. Plant Soil 366:287–303

    Article  Google Scholar 

  • Leppälammi-Kujansuu J, Salema M, Kleja DB, Linder S, Helmisaari HS (2014) Fine root turnover and litter production of Norway spruce in a long-term temperature and nutrient manipulation experiment. Plant Soil 374:73–88

    Article  Google Scholar 

  • Li YY, Liu JX, Zhou GY, Huang WJ, Duan HL (2016) Warming effects on photosynthesis of subtropical tree species: a translocation experiment along an altitudinal gradient. Sci Rep 6:24895. doi:10.1038/srep24895

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu JX, Huang WJ, Zhou GY, Zhang DQ, Liu SZ, Li YY (2013) Nitrogen to phosphorus ratios of tree species in response to elevated carbon dioxide and nitrogen addition in subtropical forests. Glob Chang Biol 19:208–216

    Article  PubMed  Google Scholar 

  • Lü XT, Cui Q, Wang QB, Han XG (2011) Nutrient resorption response to fire and nitrogen addition in a semi-arid grassland. Ecol Eng 37:534–538

    Article  Google Scholar 

  • Lü XT, Reed S, Yu Q, He NP, Wang ZW, Han XG (2013) Convergent responses of nitrogen and phosphorus resorption to nitrogen inputs in a semiarid grassland. Glob Chang Biol 19:2775–2784

    Article  PubMed  Google Scholar 

  • Lü XT, Reed SC, Yu Q, Han XG (2016) Nutrient resorption helps drive intra-specific coupling of foliar nitrogen and phosphorus under nutrient-enriched conditions. Plant Soil 398:111–120

    Article  Google Scholar 

  • Ma LN, Lü XT, Liu Y, Guo JX, Zhang NY, Yang JQ, Wang RZ (2011) The effects of warming and nitrogen addition on soil nitrogen cycling in a temperate grassland, Northeastern China. PLoS ONE 6, e27645. doi:10.1371/journal.pone.0027645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  Google Scholar 

  • Mayor JR, Mack MC, Schuur EAG (2015) Decoupled stoichiometric, isotopic, and fungal responses of an ectomycorrhizal black spruce forest to nitrogen and phosphorus additions. Soil Biol Biochem 88:247–256

    Article  CAS  Google Scholar 

  • Mayor JR, Wright SJ, Schuur EAG, Brooks ME, Turner BL (2014a) Stable nitrogen isotope patterns of trees and soils altered by long-term nitrogen and phosphorus addition to a lowland tropical rainforest. Biogeochemistry 119:293–306

    Article  CAS  Google Scholar 

  • Mayor JR, Wright SJ, Turner BL (2014b) Species-specific responses of foliar nutrients to long-term nitrogen and phosphorus additions in a lowland tropical forest. J Ecol 102:36–44

    Article  CAS  Google Scholar 

  • Melillo JM, Butle S, Johnson J, Mohan J, Steudler P, Lux H, Burrows E, Bowles F, Smith R, Scott L, Vario C, Hill T, Burton A, Zhou YM, Tang J (2011) Soil warming, carbon-nitrogen interactions, and forest carbon budgets. PANS 108:9508–9512

    Article  CAS  Google Scholar 

  • Miatto RC, Wright IJ, Batalha MA (2016) Relationships between soil nutrient status and nutrient-related leaf traits in Brazilian cerrado and seasonal forest communities. Plant Soil. doi:10.1007/s11104-016-2796-2

    Google Scholar 

  • Michener R, Lajtha K (2008) Sources of Variation in the Stable Isotopic Composition of Plants// Stable Isotopes in Ecology and Environmental Science, Second Edition. Blackwell Publishing Ltd: 22–60

  • Miller AJ, Schuur EAG, Chadwick OA (2001) Redox control of phosphorus pools in Hawaiian montane forest soils. Geoderma 102:219–237

    Article  CAS  Google Scholar 

  • Mo QF, Zou B, Li YW, Chen Y, Zhang WX, Mao R, Ding YZ, Wang J, Lu XK, Li XB, Tang JW, Li ZA, Wang FM (2015) Response of plant nutrient stoichiometry to fertilization varied with tissues in a tropical forest. Sci Rep 5. doi:10.1038/srep14605

  • Pan FJ, Zhang W, Liu SJ, Li DJ, Wang KL (2015) Leaf N: P stoichiometry across plant functional groups in the karst region of southwestern China. Trees 29:883–892

    Article  CAS  Google Scholar 

  • Peñuelas J, Sardans J, Riva-Ubach A, Janssens IA (2012) The human-induced imbalance between C, N and P in earth’s life system. Glob Chang Biol 18:3–6

    Article  Google Scholar 

  • Persson J, Fink P, Goto A, Hood JM, Jonas J, Kato S (2010) To be or not to be what you eat: regulation of stoichiometric homeostasis among autotrophs and heterotrophs. Oikos 119:741–751

    Article  CAS  Google Scholar 

  • Reed SC, Townsend AR, Davidson EA, Cleveland CC (2012) Stoichiometric patterns in foliar nutrient resorption across multiple scales. New Phytol 196:173–180

    Article  CAS  PubMed  Google Scholar 

  • Santiago LS, Wright SJ, Harms KE, Yavitt JB, Korine C, Garcia MN, Turner BL (2012) Tropical tree seedling growth responses to nitrogen, phosphorus and potassium addition. J Ecol 100:309–316

    Article  CAS  Google Scholar 

  • Sardans J, Rivas-Ubach A, Peñuelas J (2012) The C: N: P stoichiometry of organisms and ecosystems in a changing world: a review and perspectives. Perspect Plant Ecol Evol Syst 14:33–47

    Article  Google Scholar 

  • Sardans J, Peñuelas J, Estiarte M (2006) Warming and drought alter soil phosphatase activity and soil P availability in a Mediterranean shrubland. Plant Soil 289:227–238

    Article  CAS  Google Scholar 

  • Schreeg LA, Santiago LS, Wright SJ, Turner BL (2014) Stem, root, and older leaf N: P ratios are more responsive indicators of soil nutrient availability than new foliage. Ecology 95:2062–2068

    Article  CAS  PubMed  Google Scholar 

  • Sendall KM, Reich PB, Zhao CM, Hou JH, Wei XR, Stefanski A, Rice K, Rich RL, Montgomery RA (2015) Acclimation of photosynthetic temperature optima of temperate and boreal tree species in response to experimental forest warming. Glob Chang Biol 21:1342–1357

    Article  PubMed  Google Scholar 

  • Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, Princeton, pp 46–55

    Google Scholar 

  • Tu C, Booker FL, Watson DM, Chen X, Rufty TW, Shi W, Hu S (2006) Mycorrhizal mediation of plant N acquisition and residue decomposition: impact of mineral N inputs. Glob Chang Biol 12:793–803

    Article  Google Scholar 

  • Vallano DM, Sparks JP (2013) Foliar δ15N is affected by foliar nitrogen uptake, soil nitrogen, and mycorrhizae along a nitrogen deposition gradient. Oecologia 172:47–58

    Article  PubMed  Google Scholar 

  • van der Sleen P, Groenendijk P, Vlam M, Anten NPR, Boom A, Bongers F, Pons TL, Terburg G, Zuidema PA (2015) No growth stimulation of tropical trees by 150 years of CO2 fertilization but water-use efficiency increased. Biomaterials 8:5221–5230

    Google Scholar 

  • Venterink HO, Wassen MJ, Verkroost AWM, de Ruiter PC (2003) Species richness-productivity patterns differ between N-, P- and K- limited wetlands. Ecology 84:2191–2199

    Article  Google Scholar 

  • Vergutz L, Manzoni S, Porporato A, Novais RF, Jackson RB (2012) Global resorption efficiencies and concentrations of carbon and nutrients in terrestrial plants. Ecol Monogr 82:205–220

    Article  Google Scholar 

  • Wang XG, Lü XT, Han XG (2014a) Responses of nutrient concentrations and stoichiometry of senesced leaves in dominant plants to nitrogen addition and prescribed burning in a temperate steppe. Ecol Eng 70:154–161

    Article  Google Scholar 

  • Wang M, Murphy MT, Moore TR (2014b) Nutrient resorption of two evergreen shrubs in response to long-term fertilization in a bog. Oecologia 174:365–377

    Article  PubMed  Google Scholar 

  • Wang KH, Zhang XZ, Ervin E (2012) Antioxidative responses in roots and shoots of creeping bentgrass under high temperature: Effects of nitrogen and cytokinin. J Plant Physiol 169:492–500

    Article  CAS  PubMed  Google Scholar 

  • Way DA, Oren R (2010) Differential responses to changes in growth temperature between trees from different functional groups and biomes: a review and synthesis of data. Tree Physiol 30:669–688

    Article  PubMed  Google Scholar 

  • Wei CZ, Yu Q, Bai E, Lü XT, Li Q, Xia JY, Kardol P, Liang WJ, Wang ZW, Han XG (2013) Nitrogen deposition weakens plant-microbe interactions in grassland ecosystems. Glob Chang Biol 19:3688–3697

    Article  PubMed  Google Scholar 

  • Yan ZB, Kim NY, Han WX, Guo YL, Han TS, Du EZ, Fang JY (2015) Effects of nitrogen and phosphorus supply on growth rate, leaf stoichiometry, and nutrient resorption of Arabidopsis thaliana. Plant Soil 388:147–155

    Article  CAS  Google Scholar 

  • Yuan ZY, Chen HYH (2015) Decoupling of nitrogen and phosphorus in terrestrial plants associated with global changes. Nat Clim Chang 5:465–469

    Article  CAS  Google Scholar 

  • Zhang QF, Xie JS, Chen NS, Chen T, Lü MK, Zhang H, Yang YS (2016) Effects of ecological restoration on stoichiometric characteristics and nutrient resorption efficiency of Pinus massoniana foliage. Acta Ecol Sin. doi:10.5846/stxb201510182100

    Google Scholar 

  • Zhao CZ, Liu Q (2012) Effects of soil warming and nitrogen fertilization on leaf physiology of Pinus tabulaeformis seedlings. Acta Physiol Plant 34:1837–1846

    Article  CAS  Google Scholar 

  • Zheng LJ, Huang ZQ, He ZM, Wang XY, Liu ZM, Liu RQ, Xiao HY (2015) Influence of forest and foliar ages on the composition of stable carbon and nitrogen isotope of Cunninghamia lanceolata in subtropical China. Sci Silvae Sin 51:22–28

    Google Scholar 

Download references

Acknowledgments

The research was funded by the National “973” Program of China (No. 2014CB954003), the National Natural Science Foundation of China (No. 31130013), and Fujian Provincial Department of Science and Technology (No. 2016R1032–2).

Author information

Authors and Affiliations

  1. College of Geographical Science, Fujian Normal University, Fuzhou, 350007, China

    Qiufang Zhang, Jinsheng Xie, Maokui Lyu, Decheng Xiong, Jian Wang, Yuehmin Chen, Yiqing Li & Yusheng Yang

  2. State Key Laboratory of Subtropical Mountain Ecology (Funded by Ministry of Science and Technology and Fujian Province), Fujian Normal University, Fuzhou, 350007, China

    Qiufang Zhang, Jinsheng Xie, Maokui Lyu, Decheng Xiong, Jian Wang, Yuehmin Chen, Yiqing Li & Yusheng Yang

  3. Institute of Geography, Fujian Normal University, Fuzhou, 350007, China

    Jinsheng Xie, Yuehmin Chen, Yiqing Li & Yusheng Yang

  4. Department of Agricultural Chemistry, National Taiwan University, Taipei, 10617, Taiwan

    Mingkuang Wang

Authors
  1. Qiufang Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jinsheng Xie
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Maokui Lyu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Decheng Xiong
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jian Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yuehmin Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yiqing Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Mingkuang Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Yusheng Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Yuehmin Chen or Yusheng Yang.

Additional information

Responsible Editor: Jeffrey Walck.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, Q., Xie, J., Lyu, M. et al. Short-term effects of soil warming and nitrogen addition on the N:P stoichiometry of Cunninghamia lanceolata in subtropical regions. Plant Soil 411, 395–407 (2017). https://doi.org/10.1007/s11104-016-3037-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-016-3037-4

Keywords

Search

Navigation