Please wait a minute...
Journal of Arid Land  2021, Vol. 13 Issue (10): 1041-1053    DOI: 10.1007/s40333-021-0080-7
Research article     
Effect of nitrogen and phosphorus addition on leaf nutrient concentrations and nutrient resorption efficiency of two dominant alpine grass species
LIU Yalan1,2,3, LI Lei1,2,*(), LI Xiangyi1,2, YUE Zewei1,2,3, LIU Bo4
1State Key Laboratory of Desert and Oasis Ecology, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi 830011, China
2Cele National Station of Observation and Research for Desert Grassland Ecosystems, Cele 848300, China
3University of Chinese Academy of Sciences, Beijing 100049, China
4Shandong Provincial Key Laboratory of Soil Conservation and Environmental Protection, College of Resources and Environment, Linyi University, Linyi 276000, China
Download: HTML     PDF(605KB)
Export: BibTeX | EndNote (RIS)      


Nitrogen (N) and phosphorus (P) are two essential nutrients that determine plant growth and many nutrient cycling processes. Increasing N and P deposition is an important driver of ecosystem changes. However, in contrast to numerous studies about the impacts of nutrient addition on forests and temperate grasslands, how plant foliar stoichiometry and nutrient resorption respond to N and P addition in alpine grasslands is poorly understood. Therefore, we conducted an N and P addition experiment (involving control, N addition, P addition, and N+P addition) in an alpine grassland on Kunlun Mountains (Xinjiang Uygur Autonomous Region, China) in 2016 and 2017 to investigate the changes in leaf nutrient concentrations (i.e., leaf N, Leaf P, and leaf N:P ratio) and nutrient resorption efficiency of Seriphidium rhodanthum and Stipa capillata, which are dominant species in this grassland. Results showed that N addition has significant effects on soil inorganic N (NO3--N and NH4+-N) and leaf N of both species in the study periods. Compared with green leaves, leaf nutrient concentrations and nutrient resorption efficiency in senesced leaves of S. rhodanthum was more sensitive to N addition, whereas N addition influenced leaf N and leaf N:P ratio in green and senesced leaves of S. capillata. N addition did not influence N resorption efficiency of the two species. P addition and N+P addition significantly improved leaf P and had a negative effect on P resorption efficiency of the two species in the study period. These influences on plants can be explained by increasing P availability. The present results illustrated that the two species are more sensitive to P addition than N addition, which implies that P is the major limiting factor in the studied alpine grassland ecosystem. In addition, an interactive effect of N+P addition was only discernable with respect to soil availability, but did not affect plants. Therefore, exploring how nutrient characteristics and resorption response to N and P addition in the alpine grassland is important to understand nutrient use strategy of plants in terrestrial ecosystems.

Key wordsleaf nutrient concentration      nutrient resorption efficiency      leaf N:P ratio      N addition      P addition      Seriphidium rhodanthum      Stipa capillata     
Received: 13 January 2021      Published: 10 October 2021
Corresponding Authors: LI Lei     E-mail:
Cite this article:

LIU Yalan, LI Lei, LI Xiangyi, YUE Zewei, LIU Bo. Effect of nitrogen and phosphorus addition on leaf nutrient concentrations and nutrient resorption efficiency of two dominant alpine grass species. Journal of Arid Land, 2021, 13(10): 1041-1053.

URL:     OR

Fig. 1 Monthly air temperature (a) and monthly precipitation (b) in 2016 and 2017
Parameter Year N addition P addition N+P addition
Soil inorganic N <0.001*** <0.001*** 0.211 0.240
Soil available P <0.001*** 0.842 <0.001*** 0.008**
Table 1  P-values from linear mixed models for soil inorganic nitrogen (N) and soil available phosphorus (P)
Fig. 2 Responses of NH4+-N (a), NO3--N (b), soil inorganic N (c), and soil available P (d) to the four treatments (control, N addition, P addition, and N+P addition). Different uppercase letters indicate the significant differences among the four treatments in 2016, and different lowercase letters indicate the significant differences among the four treatments in 2017 (P<0.05). Bars mean standard errors.
Parameter S. rhodanthum
Green leaves Senesced leaves
Leaf N Leaf P Leaf N:P ratio Leaf N Leaf P Leaf N:P ratio
Year <0.001*** 0.051 <0.001*** 0.112 0.022* 0.480
N addition 0.005** 0.670 0.540 0.023* 0.660 0.007**
P addition 0.221 0.001** 0.573 0.651 0.001** 0.001**
N+P addition 0.243 0.771 0.772 0.354 0.842 0.078
Table 2 P-values from linear mixed models for leaf nutrient characteristics of Seriphidium rhodanthum
Parameter S. capillata
Green leaves Senesced leaves
Leaf N Leaf P Leaf N:P ratio Leaf N Leaf P Leaf N:P ratio
Year <0.001*** <0.001*** 0.711 <0.001*** <0.001*** <0.001***
N addition 0.002*** 0.922 <0.001*** <0.001*** 0.552 <0.001***
P addition 0.442 <0.001*** <0.001*** 0.362 <0.001*** <0.001***
N+P addition 0.431 0.792 0.063 0.523 0.451 0.008**
Table 3 P-values from linear mixed models for leaf nutrient characteristics of Stipa capillata
Fig. 4 N:P ratio in green and senesced leaves of S. rhodanthum and S. capillata in response to the four treatments in 2016 (a, c) and 2017 (b, d). Different uppercase letters indicate the significant differences among the four treatments in S. rhodanthum, and different lowercase letters indicate the significant differences among the four treatments in S. capillata (P<0.05). Bars mean standard errors.
Fig. 3 N and P concentrations in green and senesced leaves of Seriphidium rhodanthum and Stipa capillata in response to the four treatments in 2016 (a, c, e, g) and 2017 (b, d, f, h). Different uppercase letters indicate the significant differences among the four treatments in S. rhodanthum, and different lowercase letters indicate the significant differences among the four treatments in S. capillata (P<0.05). Bars mean standard errors.
Parameter S. rhodanthum S. capillata
Year 0.006** 0.003** <0.001*** 0.962 <0.001*** <0.001***
N addition 0.683 0.531 0.811 0.073 0.291 0.054*
P addition 0.122 0.021* 0.019* 0.522 <0.001*** 0.011*
N+P addition 0.791 0.906 0.713 0.790 0.359 0.443
Table 4 P-values from linear mixed models for nutrient resorption efficiency of S. rhodanthum and S. capillata
Fig. 5 NRE, PRE, and NRE:PRE ratio of S. rhodanthum and S. capillata in response to the four treatments in 2016 (a, c, e) and 2017 (b, d, f). NRE, nutrient resorption efficiency; PRE, phosphorus resorption efficiency. Different uppercase letters indicate the significant differences among the four treatments in S. rhodanthum, and different lowercase letters indicate the significant differences among the four treatments in S. capillata (P<0.05). Bars mean standard errors.
Species Year Leaf nutrient concentration Soil nutrient concentration
Soil inorganic N Soil available P
S. rhodanthum 2016 Green leaf N 0.30 0.27
Green leaf P -0.39 0.76**
Green leaf N:P ratio -0.09 -0.12
Senesced leaf N -0.09 -0.45
Senesced leaf P -0.24 -0.84**
Senesced leaf N:P ratio 0.56* -0.74*
2017 Green leaf N 0.23 -0.08
Green leaf P -0.17 0.53**
Green leaf N:P ratio 0.26 -0.64*
Senesced leaf N -0.39 -0.46
Senesced leaf P -0.49 -0.82**
Senesced leaf N:P ratio 0.62* -0.63*
S. capillata 2016 Green leaf N 0.65** -0.85
Green leaf P -0.24 0.68**
Green leaf N:P ratio 0.54* -0.61*
Senesced leaf N 0.69** -0.12
Senesced leaf P -0.45 0.68**
Senesced leaf N:P ratio 0.43 -0.67**
2017 Green leaf N 0.50* 0.26
Green leaf P -0.45 0.71**
Green leaf N:P ratio 0.58 -0.74**
Senesced leaf N 0.52* -0.33
Senesced leaf P -0.14 0.73**
Senesced leaf N:P ratio 0.27 -0.70**
Table 5 Correlation coefficients between leaf nutrient concentrations and soil nutrient concentrations for S. rhodanthum and S. capillata in 2016 and 2017
[1]   Aerts R. 1996. Nutrient resorption from senescing leaves of perennials: are there general patterns? Journal of Ecology, 84(4):597-608.
doi: 10.2307/2261481
[2]   Bai Y F, Wu J G, Clark C M, et al. 2010. Tradeoffs and thresholds in the effects of nitrogen addition on biodiversity and ecosystem functioning: evidence from inner Mongolia Grasslands. Global Change Biology, 16(1):358-372.
doi: 10.1111/(ISSN)1365-2486
[3]   Bobbink R. 1991. Effects of nutrient enrichment in Dutchchalk grassland. Journal of Applied Ecology, 28(1):28-41.
doi: 10.2307/2404111
[4]   Bowman W D, Theodose T A, Schardt J C, et al. 1993. Constraints of nutrient availability on primary production in two alpine tundra communities. Ecology, 74(7):2085-2097.
doi: 10.2307/1940854
[5]   Bowman W D, Gartner J R, Holland K, et al. 2006. Nitrogen critical loads for alpine vegetation and terrestrial ecosystem response: are we there yet? Ecological Applications, 16(3):1183-1193.
doi: 10.1890/1051-0761(2006)016[1183:NCLFAV]2.0.CO;2
[6]   Brant A N, Chen H Y H. 2015. Patterns and mechanisms of nutrient resorption in plants. Critical reviews in plant sciences, 34(5):471-486.
doi: 10.1080/07352689.2015.1078611
[7]   Chen F S, Niklas K J, Chen G S, et al. 2012. Leaf traits and relationships differ with season as well as among species groupings in a managed Southeastern China forest landscape. Plant Ecology, 213(9):1489-1502.
doi: 10.1007/s11258-012-0106-5
[8]   Chen F S, Niklas K J, Liu Y, et al. 2015. Nitrogen and phosphorus additions alter nutrient dynamics but not resorption efficiencies of Chinese fir leaves and twigs differing in age. Tree Physiology, 35(10):1106-1117.
doi: 10.1093/treephys/tpv076
[9]   Delonge M, D'Odorico P, Lawrence D. 2008. Feedbacks between phosphorus deposition and canopy cover: the emergence of multiple stable states in tropical dry forests. Global Change Biology, 14(1):154-160.
doi: 10.1111/gcb.2008.14.issue-1
[10]   Deng M F, Liu L L, Sun Z Z, et al. 2016. Increased phosphate uptake but not resorption alleviates phosphorus deficiency induced by nitrogen deposition in temperate Larix principis-rupprechtii plantations. New Phytologist, 212(4):1019-1029.
doi: 10.1111/nph.2016.212.issue-4
[11]   Lü X T, Reed S, Yu Q, et al. 2013. Convergent responses of nitrogen and phosphorus resorption to nitrogen inputs in a semiarid grassland. Global Change Biology, 19(9):2775-2784.
doi: 10.1111/gcb.2013.19.issue-9
[12]   Elser J J, Bracken M E S, Cleland E E, et al. 2007. Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecology Letters, 10(12):1135-1142.
doi: 10.1111/ele.2007.10.issue-12
[13]   Elser J J, Anderson T, Bergström A K, et al. 2009. Shifts in lake N:P stoichiometry and nutrient limitation driven by atmospheric nitrogen deposition. Science, 326(5954):835-837.
doi: 10.1126/science.1176199
[14]   Feller I C, McKee K L, Whigham D F, et al. 2003. Nitrogen vs. phosphorus limitation across an ecotonal gradient in a mangrove forest. Biogeochemistry, 62(2):145-175.
doi: 10.1023/A:1021166010892
[15]   Fornara D A, Banin L, Crawley M J. 2013. Multi-nutrient vs nitrogen-only effects on carbon sequestration in grassland soils. Global Change Biology, 19(12):3848-3857.
doi: 10.1111/gcb.12323 pmid: 23907927
[16]   Garnier E. 1998. Interspecific variation in plasticity of grasses in response to nitrogen supply. In: Population Biology of Grasses. Cambridge: Cambridge University Press, 155-181.
[17]   Güsewell S. 2004. N:P ratios in terrestrial plants: variation and function significance. New phytologist, 168(2):377-385.
doi: 10.1111/nph.2005.168.issue-2
[18]   Güsewell S. 2005. High nitrogen: phosphorus ratios reduce nutrient retention and second-year growth of wetland sedges. New Phytologist, 166(2):537-550.
doi: 10.1111/nph.2005.166.issue-2
[19]   He J S, Wang L, Flynn D F B, et al. 2008. Leaf nitrogen: phosphorus stoichiometry across Chinese grassland biomes. Oecologia, 155:301-310.
doi: 10.1007/s00442-007-0912-y
[20]   Huang J, Yu H, Lin H, et al. 2016. Phosphorus amendment mitigates nitrogen addition-induced phosphorus limitation in two plant species in a desert steppe, China. Plant and Soil, 399(1-2):221-232.
doi: 10.1007/s11104-015-2649-4
[21]   Jin X M, Yang L X, Yang X G, et al. 2020. Effects of N and P fertilization on the biomass and ecological stoichiometric characteristics of Agropyron michnoi in sandy grasslands. Chemistry and Ecology, 36(10):938-952.
doi: 10.1080/02757540.2020.1821672
[22]   Killingbeck K T. 1996. Nutrients in senesced leaves: keys to the search for potential resorption and resorption proficiency. Ecology, 77(6):1716-1727.
doi: 10.2307/2265777
[23]   Koerselman W, Meuleman A F. 1996. The vegetation N:P ratio: A new tool to detect the nature of nutrient limitation. Journal of Applied Ecology, 33(6):1441-1450.
doi: 10.2307/2404783
[24]   Lawrence D. 2001. Nitrogen and phosphorus enhance growth and luxury consumption of four secondary forest tree species in Borneo. Journal of Tropical Ecology, 17(6):859-869.
doi: 10.1017/S0266467401001638
[25]   Li L, Gao X P, Li X Y, et al. 2016. Nitrogen (N) and phosphorus (P) resorption of two dominant alpine perennial grass species in response to contrasting N and P availability. Environmental and Experimental Botany, 127:37-44.
doi: 10.1016/j.envexpbot.2016.03.008
[26]   Li Y, Niu S, Yu G. 2016. Aggravated phosphorus limitation on biomass production under increasing nitrogen loading: a meta-analysis. Global Change Biology, 22(2):934-943.
doi: 10.1111/gcb.13125
[27]   Liu J X, Huang W J, Zhou G Y, et al. 2013. Nitrogen to phosphorus ratios of tree species in response to elevated carbon dioxide and nitrogen addition in substropical forest. Global Change Biology, 19(1):208-216.
doi: 10.1111/gcb.12022
[28]   Long M, Wu H H, Smith M D, et al. 2016. Nitrogen deposition promotes phosphorus uptake of plants in a semi-arid temperate grassland. Plant and Soil, 408(1-2):475-484.
doi: 10.1007/s11104-016-3022-y
[29]   Marklein A R, Houlton B Z. 2012. Nitrogen inputs accelerate phosphorus cycling rates across a wide variety of terrestrial ecosystems. New Phytologist, 193(3):696-704.
doi: 10.1111/j.1469-8137.2011.03967.x pmid: 22122515
[30]   Mayor J R, Wright S J, Turner B L. 2014. Species-specific responses of foliar nutrients to long term nitrogen and phosphorus additions in a lowland tropical forest. Journal of Ecology, 102(1):36-44.
doi: 10.1111/jec.2013.102.issue-1
[31]   Menge D N L, Field C B. 2007. Simulated global changes alter phosphorus demand in annual grassland. Global Change Biology. 13(12):2582-2591.
doi: 10.1111/gcb.2007.13.issue-12
[32]   Monuca W, Kathryn B, Eric W, et al. 2021. Response of fungal endophyte communities within Andropogon gerardii (Big bluestem) to nutrient addition and herbivore exclusion. Fungal Ecology, 51:10143, doi: 10.1016/j.funeco.2021.101043.
doi: 10.1016/j.funeco.2021.101043
[33]   Ostertag R. 2010. Foliar nitrogen and phosphorus accumulation responses after fertilization: an example from nutrient-limited Hawaiian forests. Plant and Soil, 334(1-2):85-98.
doi: 10.1007/s11104-010-0281-x
[34]   Peng Y F, Peng Z P, Zeng X T, et al. 2019. Effects of nitrogen-phosphorus imbalance on plant biomass production: a global perspective. Plant and Soil, 436(1-2):245-252.
doi: 10.1007/s11104-018-03927-5
[35]   Peñuelas J, Poulter B, Sardans J, et al. 2013. Human-induced nitrogen-phosphorus imbalances alter natural and managed ecosystems across the globe. Nature Communications, 4:2934, doi: 10.1038/ncomms3934.
doi: 10.1038/ncomms3934 pmid: 24343268
[36]   Persson J, Fink P, Goto A, et al. 2010. To be or not to be what you eat: regulation of stoichiometric homeostasis among autotrophs and heterotrophs. Oikos, 119(5):741-751.
doi: 10.1111/j.1600-0706.2009.18545.x
[37]   Rodríguez H, Fraga R. 1999. Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnology Advances, 17(4):319-339.
doi: 10.1016/S0734-9750(99)00014-2
[38]   Sardans J, Rivas-Ubac A, Peñuelas J. 2012. The C:N:P stoichiometry of organisms and ecosystems in a changing world: A review and perspectives. Perspectives in Plant Ecology, Evolution and Systematics, 14(1):33-47.
doi: 10.1016/j.ppees.2011.08.002
[39]   Sword S M A, Goelz J C G, Chamber J L, et al. 2004. Long-term trends in loblolly pine productivity and stand characteristics in response to thinning and fertilization in the West Gulf region. Forest Ecology and Management, 192(1):71-96.
doi: 10.1016/j.foreco.2004.01.006
[40]   Tian D S, Niu S L. 2015. A global analysis of soil acidification caused by nitrogen addition. Environmental Research Letters, 10(2):19-24.
[41]   Tilman D. 1982. Resource Competition and Community Structure. Princeton: Princeton University Press.
[42]   Venterink H O, Vliet Revd, Wassen M J. 2001. Nutrient limitation along a productivity gradient in wet meadows. Plant and Soil, 234(2):171-179.
doi: 10.1023/A:1017922715903
[43]   Vergutz L, Manzoni S, Porporato A, et al. 2012. Global resorption efficiencies and concentrations of carbon and nutrients in leaves of terrestrial plants. Ecological Monographs, 82(2):205-220.
doi: 10.1890/11-0416.1
[44]   Wang X, Guppy C N, Watson L, et al. 2011. Availability of sparingly soluble phosphorus sources to cotton (Gossypium hirsutum L.), wheat (Triticum aestivum L.) and white lupin (Lupinus albus L.) with different forms of nitrogen as evaluated by a32P isotopic dilution technique. Plant and Soil, 348(1-2):85-98.
doi: 10.1007/s11104-011-0901-0
[45]   Wright I J, Westoby M. 2003. Nutrient concentration, resorption and lifespan: leaf traits of Australian sclerophyll species. Function Ecology, 17(1):10-19.
doi: 10.1046/j.1365-2435.2003.00694.x
[46]   Xu L, Xing A, Du E, et al. 2021. Effects of nitrogen addition on leaf nutrient stoichiometry in an old-growth boreal forest. Ecosphere, 12(1): ecs2.3335, doi: 10.1002/ecs2.3335.
doi: 10.1002/ecs2.3335
[47]   Xu X, Timmer V R. 1999. Growth and nitrogen nutrition of Chinese fir seedlings exposed to nutrient loading and fertilization. Plant and Soil, 216(1-2):83-91.
doi: 10.1023/A:1004733714217
[48]   Xu X, Wanek W, Zhou C, et al. 2014. Nutrient limitation of alpine plants: Implications from leaf N:P stoichiometry and leaf δ15N. Journal of Plant Nutrient and Soil Science, 177(3):378-387.
[49]   Yang H. 2018. Effects of nitrogen and phosphorus addition on leaf nutrient characteristics in a subtropical forest. Trees, 32(2):383-391.
doi: 10.1007/s00468-017-1636-1
[50]   Yuan Z Y, Chen H Y H. 2009. Global-scale patterns of nutrient resorption associated with latitude, temperature and precipitation. Global Ecology and Biogeography, 18(1):11-18.
doi: 10.1111/geb.2009.18.issue-1
[51]   Yuan Z Y, Chen H Y H. 2015. Negative effects of fertilization on plant nutrient resorption. Ecology, 96(2):373-380.
pmid: 26240859
[52]   Yue P, Li K, Gong Y, et al. 2016. A five-years study of the impact of nitrogen addition on methane uptake in alpine grassland. Scientific Reports, 6:32064, doi: org/10.1038/srep32064.
doi: org/10.1038/srep32064
[53]   Zhang D, Hui D, Luo Y, et al. 2008. Rates of litter decomposition in terrestrial ecosystems: global patterns and controlling factors. Journal of Plant Ecology, 1(2):85-93.
doi: 10.1093/jpe/rtn002
[54]   Zhang L X, Bai Y F, Han X G. 2004. Differential response of N:P stoichiometry of Leymus chinensis and Carex Korshinskyi to N additions in a steppe ecosystem in Nei Mongol. Acta Botanica Sinica, 46(3):259-270.
[55]   Zhang Q F, Xie J S, Lyu M, et al. 2017. Short-term effects of soil warming and nitrogen addition on the N:P stoichiometry of Cunninghamia lanceolata in subtropical regions. Plant and Soil, 411(1-2):395-407.
doi: 10.1007/s11104-016-3037-4
[56]   Zhang X Y, Jia J, Chen L T, et al. 2021. Aridity and NPP constrain contribution of microbial necromass to soil organic carbon in the Qinghai-Tibet alpine grasslands. Soil Biology and Biochemistry, 156:108213, doi: 10.1016/j.soilbio.2021.108213.
doi: 10.1016/j.soilbio.2021.108213
[57]   Zheng L L, Zhao Q, Sun Q Y, et al. 2020. Nitrogen addition elevated autumn phosphorus retranslocation of living needles but not resorption in a nutrient-poor Pinus sylvestris var. Mongolica plantation. Forest Ecology and Management, 468:118174, doi: 10.1016/j.foreco.2020.118174.
doi: 10.1016/j.foreco.2020.118174
[58]   Zhao G S, Shi P L, Wu J S, et al. 2017. Foliar nutrient resorption patterns of four functional plants along a precipitation gradient on the Tibetan Changtang Plateau. Ecology and Evolution, 7(18):7201-7212.
doi: 10.1002/ece3.2017.7.issue-18
[1] SU Yuan, MA Xiaofei, GONG Yanming, LI Kaihui, HAN Wenxuan, LIU Xuejun. Contrasting effects of nitrogen addition on litter decomposition in forests and grasslands in China[J]. Journal of Arid Land, 2021, 13(7): 717-729.
[2] LianLian FAN, Yan LI, LiSong TANG, Jian MA. Combined effects of snow depth and nitrogen addition on ephemeral growth at the southern edge of the Gurbantunggut Desert, China[J]. Journal of Arid Land, 2013, 5(4): 500-510.
[3] Ling SONG, XueMei BAO, XueJun LIU, FuSuo ZHANG. Impact of nitrogen addition on plant community in a semi-arid temperate steppe in China[J]. Journal of Arid Land, 2012, 4(1): 3-10.