Abstract
Aims
Foliar nutrient resorption is a critical process for considerations of ecosystem nutrient cycles. Previous studies have described the independent effects of climatic factors, plant and soil nutrient status on nutrient resorption. However, little is known about the comprehensive effects of these factors on nutrient resorption, especially based on observations in situ.
Methods
In a semi-arid grassland of the Loess Plateau, China, we conducted an eight-year field survey and sampled leaves and soils separately in 2013, 2016, and 2020. We explored interannual variation in foliar nutrient resorption efficiency (NuRE, including nitrogen and phosphorus resorption efficiency, i.e., NRE and PRE) and the driving factors in graminoids and forbs.
Results
The NuRE in graminoids varied significantly, but in forbs varied insignificantly among years, indicating a more flexible nutrient resorption strategy in graminoids. Further, climatic variables showed stronger effects on NuRE than soil nutrients. Specifically, growing-season temperature and precipitation controlled NuRE of graminoids and forbs by regulating green leaf N:P ratio ([N:P]g), while soil nutrients did not affect NuRE. The regulation of [N:P]g on NuRE was explained by foliar stoichiometric control in which N and P were resorbed proportionally with [N:P]g. Meanwhile, the positive relationships between NRE and PRE and between NRE:PRE and [N:P]g confirmed stoichiometric control on NuRE.
Conclusion
Our findings suggested that growing season hydro-thermal factors affected the interannual variations of NuRE through a foliar stoichiometric control strategy. Meanwhile, more NuRE plasticity and positive responses to climatic factors in graminoids (the dominant group here) could explain their dominance in this grassland.
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Data availability
The data that support this study are available from the corresponding author upon reasonable request.
References
Aerts R (1996) Nutrient resorption from senescing leaves of perennials: are there general patterns? J Ecol 84:597–608. https://doi.org/10.2307/2261481
Bertiller MB, Mazzarino MJ, Carrera AL, Diehl P, Satti P, Gobbi M, Sain CL (2006) Leaf strategies and soil N across a regional humidity gradient in Patagonia. Oecologia 148:612–624. https://doi.org/10.1007/s00442-006-0401-8
Brant AN, Chen HYH (2015) Patterns and mechanisms of nutrient resorption in plants. Crit Rev Plant Sci 34:471–486. https://doi.org/10.1080/07352689.2015.1078611
Chen YH, Han WX, Tang LY, Tang ZY, Fang JY (2013) Leaf nitrogen and phosphorus concentrations of woody plants differ in responses to climate, soil and plant growth form. Ecography 36:178–184. https://doi.org/10.1111/j.1600-0587.2011.06833.x
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 Chinese fir leaves and twigs differing in age. Tree Physiol 35:1106–1117. https://doi.org/10.1093/treephys/tpv076
Chen ZF, Xiong PF, Zhou JJ, Yang Q, Wang Z, Xu BC (2020) Grassland productivity and diversity changes in responses to N and P addition depend primarily on tall clonal and annual species in semiarid Loess Plateau. Ecol Eng 145:105727. https://doi.org/10.1016/j.ecoleng.2020.105727
Chen H, Reed SC, Lü XT, Xiao KC, Wang KL, Li DJ (2021) Coexistence of multiple leaf nutrient resorption strategies in a single ecosystem. Sci Total Environ 772:144951. https://doi.org/10.1016/j.scitotenv.2021.144951
Cheng JM, Zou H, Cheng J (2014) Grassland ecosystem of the Loess Plateau in China-Yunwushan national nature reserve. Science Press, Beijing, pp 5–21
Cornelissen JHC, Lavorel S, Garnier E, Díaz S, Buchmann N, Gurvich DE, Reich PB, Steege HT, Morgan HD, van-der-heijden MGA, Pausas JG, Poorter H (2003) A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Aust J Bot 51:335–380. https://doi.org/10.1071/BT02124
Craine JM, Nippert JB, Elmore AJ, Skibbe AM, Hutchinson SL, Brunsell NA (2012) Timing of climate variability and grassland productivity. P Natl Acad Sci USA 109:3401–3405. https://doi.org/10.1073/pnas.1118438109
Craine JM, Ocheltree TW, Nippert JB, Towne EG, Skibbe AM, Kembel SW, Fargione JE (2013) Global diversity of drought tolerance and grassland climate-change resilience. Nat Clim Change 3:63–67. https://doi.org/10.1038/nclimate1634
Cui YX, Fang LC, Guo XB, Wang X, Zhang YJ, Li PF, Zhang XC (2018) Ecoenzymatic stoichiometry and microbial nutrient limitation in rhizosphere soil in the arid area of the northern Loess Plateau, China. Soil Biol Biochem 116:11–21. https://doi.org/10.1016/j.soilbio.2017.09.025
Delgado-Baquerizo M, Maestre FT, Gallardo A, Bowker MA, Wallenstein MD, Quero JL, Ochoa V, Gozalo B et al (2013) Decoupling of soil nutrient cycles as a function of aridity in global drylands. Nature 502:672–676. https://doi.org/10.1038/nature12670
Domeignoz-Horta LA, Pold G, Liu XJA, Frey SD, Melillo JM, DeAngelis KM (2020) Microbial diversity drives carbon use efficiency in a model soil. Nat Commun 11:3684. https://doi.org/10.1038/s41467-020-17502-z
Drenovsky RE, Richards JH (2004) Critical N: P values: predicting nutrient deficiencies in desert shrublands. Plant Soil 259:59–69. https://doi.org/10.1023/B:PLSO.0000020945.09809.3d
Drenovsky RE, Pietrasiak N, Short TH (2019) Global temporal patterns in plant nutrient resorption plasticity. Global Ecol Biogeogr 28:728–743. https://doi.org/10.1111/geb.12885
Du EZ, Terrer C, Pellegrini AFA, Ahlström A, van Lissa CJ, Zhao X, Xia N, Wu XH, Jackson RB (2020) Global patterns of terrestrial nitrogen and phosphorus limitation. Nat Geosci 13:221–226. https://doi.org/10.1038/s41561-019-0530-4
Du BM, Ji HW, Liu SR, Kang HZ, Yin S, Liu CJ (2021) Nutrient resorption strategies of three oak tree species in response to interannual climate variability. For Ecosyst 8:70. https://doi.org/10.1186/s40663-021-00350-8
Eckstein RL, Karlsson PS, Weih M (1999) Leaf life span and nutrient resorption as determinants of plant nutrient conservation in temperate-arctic regions. New Phytol 143:177–189. https://doi.org/10.1046/j.1469-8137.1999.00429.x
Freschet GT, Cornelissen JHC, van Logtestijn RSP, Aerts R (2010) Substantial nutrient resorption from leaves, stems and roots in a subarctic flora: what is the link with other resource economics traits? New Phytol 186:879–889. https://doi.org/10.1111/j.1469-8137.2010.03228.x
Ghiloufi W, Chaieb M (2021) Environmental factors controlling vegetation attributes, soil nutrients and hydrolases in South Mediterranean arid grasslands. Ecol Eng 161:106155. https://doi.org/10.1016/j.ecoleng.2021.106155
Guan XK, Turner NC, Song L, Gu YJ, Wang TC, Li FM (2016) Soil carbon sequestration by three perennial legume pastures is greater in deeper soil layers than in the surface soil. Biogeosciences 13:527–534. https://doi.org/10.5194/bg-13-527-2016
Güsewell S (2005) Nutrient resorption of wetland graminoids is related to the type of nutrient limitation. Funct Ecol 19:344–354. https://doi.org/10.1111/j.1365-2435.2005.00967.x
Güsewell S, Koerselman W (2002) Variation in nitrogen and phosphorus concentrations of wetland plants. Perspect Plant Ecol 5:37–61. https://doi.org/10.1078/1433-8319-0000022
Han WX, Tang LY, Chen YH, Fang JY (2013) Relationship between the relative limitation and resorption efficiency of nitrogen vs phosphorus in woody plants. PLoS One 8:e83366. https://doi.org/10.1371/journal.pone.0083366
He MS, Yan ZB, Cui XQ, Gong YM, Li KH, Han WX (2020) Scaling the leaf nutrient resorption efficiency: nitrogen vs phosphorus in global plants. Sci Total Environ 729:138920. https://doi.org/10.1016/j.scitotenv.2020.138920
Heilmeier H (2019) Functional traits explaining plant responses to past and future climate changes. Flora 254:1–11. https://doi.org/10.1016/j.flora.2019.04.004
Hou SL, Dijkstra FA, Lü XT, Han XG (2023) Increases in the dominance of species with higher N: P flexibility exacerbate community N-P imbalances following N inputs. Biogeochemistry 163:279–288. https://doi.org/10.1007/s10533-023-01033-y
Jiang CM, Yu GR, Li YN, Cao GM, Yang ZP, Sheng WP, Yu WT (2012) Nutrient resorption of coexistence species in alpine meadow of the Qinghai-Tibetan Plateau explains plant adaptation to nutrient-poor environment. Ecol Eng 44:1–9. https://doi.org/10.1016/j.ecoleng.2012.04.006
Kobe RK, Lepczyk CA, Iyer M (2005) Resorption efficiency decreases with increasing green leaf nutrients in a global data set. Ecology 86:2780–2792. https://doi.org/10.1890/04-1830
Kuznetsova T, Rosenvald K, Ostonen I, Helmisaari HS, Mandre M, Lõhmus K (2010) Survival of black alder (Alnus glutinosa L.), silver birch (Betula pendula Roth.) and Scots pine (Pinus sylvestris L.) seedlings in a reclaimed oil shale mining area. Ecol Eng 36:495–502. https://doi.org/10.1016/j.ecoleng.2009.11.019
Lambers H (2022) Annual review of plant biology phosphorus acquisition and utilization in plants. Annu Rev Plant Biol 73:17–42. https://doi.org/10.1146/annurev-arplant-102720-125738
Lefcheck JS (2016) piecewiseSEM: piecewise structural equation modelling in R for ecology, evolution, and systematics. Methods Ecol Evol 7:573–579. https://doi.org/10.1111/2041-210X.12512
Li XF, Zheng XB, Han SJ, Zheng JQ, Li TH (2010) Effects of nitrogen additions on nitrogen resorption and use efficiencies and foliar litterfall of six tree species in a mixed birch and poplar forest, northeastern China. Can J Forest Res 40:2256–2261. https://doi.org/10.1139/X10-167
Li L, Gao XP, Li XY, Lin LS, Zeng FJ, Gui DW, Lu Y (2016) Nitrogen (N) and phosphorus (P) resorption of two dominant alpine perennial grass species in response to contrasting N and P availability. Environ Exp Bot 127:37–44. https://doi.org/10.1016/j.envexpbot.2016.03.008
Li QE, Michalet R, Guo X, Xie HC, He MZ (2021) Variation in biomass and nutrients allocation of Corydalis hendersonii on the Tibetan Plateau with increasing rainfall continentality and altitude. Ecol Indic 132:108244. https://doi.org/10.1016/j.ecolind.2021.108244
Li XE, Hu YF, Zhang RY, Zhao X, Qian C (2022) Linking leaf N: P stoichiometry to species richness and composition along a slope aspect gradient in the Eastern Tibetan meadows. Diversity 14:245. https://doi.org/10.3390/d14040245
Lind EM, Borer E, Seabloom E, Adler P, Bakker JD, Blumenthal DM, Crawley M, Davies K, Firn J, Gruner DS, Stanley-harpole W, Hautier Y, Hillebrand H, Knops J, Melbourne B, Mortensen B, Risch AC, Schuetz M, Stevens C, Wragg PD (2013) Life-history constraints in grassland plant species: a growth-defence trade-off is the norm. Ecol Lett 16:513–521. https://doi.org/10.1111/ele.12078
Liu B, Gao DC, Chang Q, Liu ZP, Fan XL, Meng D, Bai E (2022) Leaf enzyme plays a more important role in leaf nitrogen resorption efficiency than soil properties along an elevation gradient. J Ecol 110:2603–2614. https://doi.org/10.1111/1365-2745.13971
Liu L, Zhao Q, Zheng LL, Zeng DH (2023) Responses of nutrient resorption to interannual precipitation variability and nitrogen addition in a pine plantation. Ecosphere 14:1–16. https://doi.org/10.1002/ecs2.4395
Lü XT, Han XG (2010) Nutrient resorption responses to water and nitrogen amendment in semi-arid grassland of Inner Mongolia, China. Plant Soil 327:481–491. https://doi.org/10.1007/s11104-009-0078-y
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. Global Change Biol 19:2775–2784. https://doi.org/10.1111/gcb.12235
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. https://doi.org/10.1007/s11104-015-2642-y
Lü XT, Hu YY, Wolf AA, Han XG (2019) Species richness mediates within-species nutrient resorption: implications for the biodiversity–productivity relationship. J Ecol 107:2346–2352. https://doi.org/10.1111/1365-2745.13180
Matías L, Hidalgo-Galvez MD, Cambrollé J, Domínguez MT, Pérez-Ramos IM (2021) How will forecasted warming and drought affect soil respiration in savannah ecosystems? the role of tree canopy and grazing legacy. Agr Forest Meteorol 304–305:108425. https://doi.org/10.1016/j.agrformet.2021.108425
Mayor JR, Wright SJ, Turner BL (2014) Species-specific responses of foliar nutrients to long-term nitrogen and phosphorus additions in a lowland tropical forest. J Ecol 102:36–44. https://doi.org/10.1111/1365-2745.12190
Mu XH, Chen YL (2021) The physiological response of photosynthesis to nitrogen deficiency. Plant Physiol Bioch 158:76–82. https://doi.org/10.1016/j.plaphy.2020.11.019
Ocheltree TW, Mueller KM, Chesus K, LeCain DR, Kray JA, Blumenthal DM (2020) Identification of suites of traits that explains drought resistance and phenological patterns of plants in a semi-arid grassland community. Oecologia 192:55–66. https://doi.org/10.1007/s00442-019-04567-x
Ordoñez JC, Van Bodegom PM, Witte JPM, Wright IJ, Reich PB, Aerts R (2009) A global study of relationships between leaf traits, climate and soil measures of nutrient fertility. Global Ecol Biogeogr 18:137–149. https://doi.org/10.1111/j.1466-8238.2008.00441.x
Peng F, Xue X, Li CY, Lai CM, Sun J, Tsubo M, Tsunekawa A, Wang T (2020) Plant community of alpine steppe shows stronger association with soil properties than alpine meadow alongside degradation. Sci Total Environ 733:139048. https://doi.org/10.1016/j.scitotenv.2020.139048
Pons TL, Westbeek MHM (2004) Analysis of differences in photosynthetic nitrogen-use efficiency between four contrasting species. Physiol Plant 122:68–78. https://doi.org/10.1111/j.13993054.2004.00380.x
Ratnam J, Sankaran M, Hanan NP, Grant C, Zambatis N (2008) Nutrient resorption patterns of plant functional groups in a tropical savanna: variation and functional significance. Oecologia 157:141–151. https://doi.org/10.1007/s00442-008-1047-5
Reed SC, Townsend AR, Davidson EA, Cleveland CC (2012) Stoichiometric patterns in foliar nutrient resorption across multiple scales. New Phytol 196:173–180. https://doi.org/10.1111/j.14698137.2012.04249.x
Reich PB, Oleksyn J (2004) Global patterns of plant leaf N and P in relation to temperature and latitude. P Natl Acad Sci USA 101:11001–11006. https://doi.org/10.1073/pnas.0403588101
Rejmánková E (2005) Nutrient resorption in wetland macrophytes: comparison across several regions of different nutrient status. New Phytol 167:471–482. https://doi.org/10.1111/j.1469-8137.2005.01449.x
Sardans J, Peñuelas J, Ogaya R (2008) Experimental drought reduced acid and alkaline phosphatase activity and increased organic extractable P in soil in a Quercus ilex Mediterranean forest. Eur J Soil Biol 44:509–520. https://doi.org/10.1016/j.ejsobi.2008.09.011
See CR, Yanai RD, Fisk MC, Vadeboncoeur MA, Quintero BA, Fahey TJ (2015) Soil nitrogen affects phosphorus recycling: foliar resorption and plant-soil feedbacks in a northern hardwood forest. Ecology 96:2488–2498. https://doi.org/10.1890/15-0188.1
Singh DK, Sale PWG, Pallaghy CK, McKenzie BM (2000) Phosphorus concentrations in the leaves of defoliated white clover affect abscisic acid formation and transpiration in drying soil. New Phytol 146:249–259. https://doi.org/10.1046/j.1469-8137.2000.00644.x
Sorrell BK, Chagué-Goff C, Basher LM, Partridge TR (2011) N: P ratios, δ15N fractionation and nutrient resorption along a nitrogen to phosphorus limitation gradient in an oligotrophic wetland complex. Aquat Bot 94:93–101. https://doi.org/10.1016/j.aquabot.2010.11.006
Sunagawa S, Coelho LP, Chaffron S, Kultima JR, Labadie K, Salazar G, Djahanschiri B, Zeller G (2015) Structure and function of the global ocean microbiome. Science 348:1261359. https://doi.org/10.1126/science.1261359
Tang LY, Han WX, Chen YH, Fang JY (2013) Resorption proficiency and efficiency of leaf nutrients in woody plants in eastern China. J Plant Ecol 6:408–417. https://doi.org/10.1093/jpe/rtt013
Tao Y, Wu GL, Zhang YM, Zhou XB (2016) Leaf N and P stoichiometry of 57 plant species in the Karamori Mountain Ungulate Nature Reserve, Xinjiang, China. J Arid Land 8:935–947. https://doi.org/10.1007/s40333-016-0019-6
Tian QY, Yang LY, Ma PF, Zhou HR, Liu NN, Bai WM, Wang H, Ren LF, Lu P, Han WW, Schultz PA, Bever JD, Zhang FS, Lambers H, Zhang WH (2020) Below-ground-mediated and phase-dependent processes drive nitrogen-evoked community changes in grasslands. J Ecol 108:1874–1887. https://doi.org/10.1111/1365-2745.13415
Tully KL, Wood TE, Schwantes AM, Lawrence D (2013) Soil nutrient availability and reproductive effort drive patterns in nutrient resorption in Pentaclethra macroloba. Ecology 94:930–940. https://doi.org/10.1890/12-0781.1
van Sundert K, Arfin-Khan MAS, Bharath S, Buckley YM, Caldeira MC, Donohue I, Dubbert M et al (2021) Fertilized graminoids intensify negative drought effects on grassland productivity. Glob Chang Biol 27:2441–2457. https://doi.org/10.1111/gcb.15583
Veldhuis MP, Hulshof A, Fokkema W, Berg MP, Olff H (2016) Understanding nutrient dynamics in an African savanna: local biotic interactions outweigh a major regional rainfall gradient. J Ecol 104:913–923. https://doi.org/10.1111/1365-2745.12569
Vergutz L, Manzoni S, Porporato A, Novais RF, Jackson RB (2012) Global resorption efficiencies and concentrations of carbon and nutrients in leaves of terrestrial plants. Ecol Monogr 82:205–220. https://doi.org/10.1890/11-0416.1
Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen phosphorus interactions. Ecol Appl 20:5–15. https://doi.org/10.1890/08-0127.1
Wang SP, Duan JC, Xu GG, Wang YF, Zhang ZH, Rui YC, Luo CY, Xu B, Zhu XX, Chang XF, Cui XY, Niu HS, Zhao XQ, Wang WY (2012) Effects of warming and grazing on soil N availability, species composition, and ANPP in an alpine meadow. Ecology 93:2365–2376. https://doi.org/10.1016/j.agrformet.2020.108278
Wang ZN, Lu JY, Yang HM, Zhang X, Luo CL, Zhao YX (2014) Resorption of nitrogen, phosphorus and potassium from leaves of lucerne stands of different ages. Plant Soil 383:301–312. https://doi.org/10.1007/s11104-014-2166-x
Wang LL, Wang L, He WL, An LZ, Xu SJ (2017) Nutrient resorption or accumulation of desert plants with contrasting sodium regulation strategies. Sci Rep-UK 7:17035. https://doi.org/10.1038/s41598-017-17368-0
Wang ZQ, Fan ZX, Zhao Q, Wan MC, Ran JZ, Huang H, Niklas KJ (2018) Global data analysis shows that soil nutrient levels dominate foliar nutrient resorption efficiency in herbaceous species. Front Plant Sci 9:1431. https://doi.org/10.3389/fpls.2018.01431
Wang XC, Chen Y, Liu F, Zhao R, Quan XK, Wang CK (2020) Nutrient resorption estimation compromised by leaf mass loss and area shrinkage: variations and solutions. Forest Ecol Manag 472:118232. https://doi.org/10.1016/j.foreco.2020.118232
Wei XR, Zhang YJ, Liu J, Gao HL, Fan J, Jia XX, Cheng JM, Shao MA, Zhang XC (2015) Response of soil CO2 efflux to precipitation manipulation in a semiarid grassland. J Environ Sci-China 45:207–214. https://doi.org/10.1016/j.jes.2016.01.008
Wright IJ, Westoby M (2003) Nutrient concentration, resorption and lifespan: leaf traits of Australian sclerophyll species. Funct Ecol 17:10–19. https://doi.org/10.1046/j.1365-2435.2003.00694.x
Xu MP, Zhu YF, Zhang SH, Feng YZ, Zhang W, Han XH (2021) Global scaling the leaf nitrogen and phosphorus resorption of woody species: revisiting some commonly held views. Sci Total Environ 788:147807. https://doi.org/10.1016/j.scitotenv.2021.147807
Yan WM, Zhong YQW, Zheng SX, Shangguan ZP (2016) Linking plant leaf nutrients stoichiometry to water use efficiency on the Loess Plateau in China. Ecol Eng 87:124–131. https://doi.org/10.1016/j.ecoleng.2015.11.034
Yan ZB, Tian D, Han WX, Tang ZY, Fang JY (2017) An assessment on the uncertainty of the nitrogen to phosphorus ratio as a threshold for nutrient limitation in plants. Ann Bot-London 120:937–942. https://doi.org/10.1093/aob/mcx106
Yan T, Zhu JJ, Yang K (2018) Leaf nitrogen and phosphorus resorption of woody species in response to climatic conditions and soil nutrients: a meta-analysis. J Forest Res 29:905–913. https://doi.org/10.1007/s11676-017-0519-z
Yang H (2018) Effects of nitrogen and phosphorus addition on leaf nutrient characteristics in a subtropical forest. Trees-Struct Funct 32:383–391. https://doi.org/10.1007/s00468-017-1636-1
Yu MF, Tao YX, Liu WZ, Xing W, Liu GH, Wang L, Ma L (2020) C, N, and P stoichiometry and their interaction with different plant communities and soils in subtropical riparian wetlands. Environ Sci Pollut R 27:1024–1034. https://doi.org/10.1007/s11356-019-07004-x
Yuan ZY, Chen HYH (2009) Global-scale patterns of nutrient resorption associated with latitude, temperature and precipitation. Global Ecol Biogeog 18:11–18. https://doi.org/10.1111/j.1466-8238.2008.00425.x
Yuan ZY, Li LH, Han XG, Huang JH, Jiang GM, Wan SQ, Zhang WH, Chen QS (2005) Nitrogen resorption from senescing leaves in 28 plant species in a semi-arid region of northern China. J Arid Environ 63:191–202. https://doi.org/10.1016/j.jaridenv.2005.01.023
Yuan ZY, Jiao F, Shi XR, Sardans J, Maestre FT, Delgado-Baquerizo M, Reich PB, Peñuelas J (2017) Experimental and observational studies find contrasting responses of soil nutrients to climate change. eLife 6:e23255. https://doi.org/10.7554/eLife.23255
Zhang JL, Zhang SB, Chen YJ, Zhang YP, Poorter L (2015a) Nutrient resorption is associated with leaf vein density and growth performance of dipterocarp tree species. J Ecol 103:541–549. https://doi.org/10.1111/1365-2745.12392
Zhang JH, Li H, Shen HH, Chen YN, Fang JY, Tang ZY (2015b) Effects of nitrogen addition on nitrogen resorption in temperate shrublands in northern China. PLoS One 10:e01130434. https://doi.org/10.1371/journal.pone.0130434
Zhang C, Liu GB, Song ZL, Wang J, Gu L (2018) Interactions of soil bacteria and fungi with plants during long-term grazing exclusion in semiarid grasslands. Soil Biol Biochem 124:47–58. https://doi.org/10.1016/j.soilbio.2018.05.026
Zhang Y, Su JS, Jing GH, Cheng JM (2022) Forbs dominate plant nutrient resorption of plant community along a 34-year grazing exclusion gradient in a semiarid grassland. Ecol Eng 175:106497. https://doi.org/10.1016/j.ecoleng.2021.106497
Zhao GS, Shi PL, Wu JS, Xiong DP, Zong N, Zhang XZ (2017) Foliar nutrient resorption patterns of four functional plants along a precipitation gradient on the Tibetan Changtang Plateau. Ecol Evol 7:7201–7212. https://doi.org/10.1002/ece3.3283
Zhu XR, Li XT, Xing F, Chen C, Huang GH, Gao Y (2020) Interaction between root exudates of the poisonous plant Stellera chamaejasme L. and arbuscular mycorrhizal fungi on the growth of Leymus chinensis (trin.) tzvel. Microorganisms 8:364. https://doi.org/10.3390/microorganisms8030364
Zong N, Shi PL, Chai X (2018) Effects of warming and nitrogen addition on nutrient resorption efficiency in an alpine meadow on the northern Tibetan Plateau. Soil Sci Plant Nutr 64:482–490. https://doi.org/10.1080/00380768.2018.1467727
Acknowledgements
We greatly appreciate Guanghua Jing, Jishuai Su, Ruimin Luo, Zhoumin Zheng, Jin Mao, and Ying Duo for help with the fieldwork and data collection. We would like to thank a native speaker from the HighEdit company for assistance with the English language editing of this manuscript.
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This project was funded by the National Natural Science Foundation of China (41701606), the Natural Science Basic Research Plan in Shaanxi Province (2021JM-093), the Youth Talent Development Program of Northwest A&F University (2452020009), the Innovation Project from Institute of Soil and Water Conservation (A315022208), and the National Key Research and Development Program of China (2016YFA0600801).
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Conceptualization and Methodology, L Guo; Data curation, WH Fu; Formal analysis, Writing – original draft preparation, and Visualization, XW Liu and WH Fu; Writing – review & editing, YQ Wang, ZY Yuan, Q Yu, CH Peng, SE Koerner, and L Guo. All authors gave final approval for publication and agreed to be held accountable for the work performed therein.
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Liu, X., Wang, Y., Fu, W. et al. Growing season temperature and precipitation affect nutrient resorption in herbaceous species through a foliar stoichiometric control strategy. Plant Soil 493, 45–60 (2023). https://doi.org/10.1007/s11104-023-06214-0
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DOI: https://doi.org/10.1007/s11104-023-06214-0