Abstract
Aims
Phosphorus (P) addition can help restore degraded Chinese grasslands. Soil P-availability affects the plant niche dynamics. However, the dynamics of niche characteristics are not yet understood, particularly for above- and belowground differences between species and plant–microbe interactions that generate these dynamics.
Methods
We conducted a long-term field P-fertilization experiment (0 to 12.5 g P m−2 year−1) to explore the impacts of P addition on the niche dynamics of a competitive forb (Chenopodium aristatum, a non-mycorrhizal C4 plant) and a dominant grass (Leymus chinensis, a mycorrhizal C3 plant) in a temperate grassland in Inner Mongolia, northern China.
Results
Phosphorus addition greatly changed the niche and exacerbated aboveground competition between C. aristatum and L. chinensis. Competitive exclusion of L. chinensis occurred at all levels, except P2.5. Photosynthesis and above- and belowground morphology of C. aristatum responded more to P1 due to its high photosynthetic plasticity and nutrient resorption, which was associated with its competitive advantage. Although NO peaked at P2.5, carbon assimilation and rhizosheath microbial biomass of L. chinensis were optimal. Alleviated NO at P5 and P12.5 was associated with segregation of root morphologies and rhizosheath microbial composition. However, surplus niches at P5 and P12.5 were occupied by invasive sub-shrubs, associating with the mismatched plant–microbe feedbacks of C. aristatum and L. chinensis.
Conclusions
Our findings suggest that rhizosheath microbes mediate trade-offs between a host plant’s P-conservation and acquisition and highlight the importance of above- and belowground co-responses to community productivity and stability under P addition.
Similar content being viewed by others
Data availability
The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.
References
Aschehoug ET, Callaway RM (2014) Morphological variability in tree root architecture indirectly affects coexistence among competitors in the understory. Ecology 95:1731–1736. https://doi.org/10.1890/13-1749.1
Ashton IW, Miller AE, Bowman WD, Suding KN (2010) Niche complementarity due to plasticity in resource use: plant partitioning of chemical N forms. Ecology 91:3252–3260. https://doi.org/10.1890/09-1849.1
Austin MP, Meyers JA (1996) Current approaches to modelling the environmental niche of eucalypts: implication for management of forest biodiversity. For Ecol Manag 85:95–106. https://doi.org/10.1016/S0378-1127(96)03753-X
Ávila-Lovera E, Goldsmith GR, Kay KM, Funk JL (2021) Above- and below-ground functional trait coordination in the neotropical understory genus Costus. AoB Plants 14:plab073. https://doi.org/10.1093/aobpla/plab073
Babalola OO, Fadiji AE, Enagbonma BJ, Alori ET, Ayilara MS, Ayangbenro AS (2020) The nexus between plant and plant microbiome: revelation of the networking strategies. Front Microbiol 11:548037. https://doi.org/10.3389/fmicb.2020.548037/full
Bai Y, Wu J, Xing Q, Pan Q, Huang J, Yang D, Han X (2008) Primary production and rain use efficiency across a precipitation gradient on the Mongolia plateau. Ecology 89:2140–2153
Bai Y, Wu J, Clark CM, Naeem S, Pan Q, Huang J, Zhang L, Han X (2010) Tradeoffs and thresholds in the effects of nitrogen addition on biodiversity and ecosystem functioning: evidence from inner Mongolia grasslands. Global Change Biol 16:358–372. https://doi.org/10.1111/j.1365-2486.2009.01950.x
Baldarelli LM, Throop HL, Collins SL, Ward D (2021) Nutrient additions have direct and indirect effects on biocrust biomass in a long-term Chihuahuan Desert grassland experiment. J Arid Environ 184:104317. https://doi.org/10.1016/j.jaridenv.2020.104317
Barazetti AR, Simionato AS, Pérez-Navarro MO, dos Santos IMO, Modolon F, de Lima Andreata MF , Liuti G, Cely MVT, Chryssafidis AL, Dealis ML, Andrade G (2019) Formulations of arbuscular mycorrhizal fungi inoculum applied to soybean and corn plants under controlled and field conditions. Appl Soil Ecol 142:25–43. https://doi.org/10.1016/j.apsoil.2019.05.015
Boisson S, Monty A, Séleck M, Shutcha MN, Faucon M, Mahy G (2020) Ecological niche distribution along soil toxicity gradients: bridging theoretical expectations and metallophyte conservation. Ecol Mod 415:108861. https://doi.org/10.1016/j.ecolmodel.2019.108861
Bossio DA, Scow KM (1998) Impacts of carbon and flooding on soil microbial communities: phospholipid fatty acid profiles and substrate utilization patterns. Microb Ecol 35:265–278. https://doi.org/10.1007/s002489900082
Brookes PC, Powlson DS, Jenkinson DS (1982) Measurement of microbial biomass phosphorus in soil. Soil Biol Biochem 14:319–329. https://doi.org/10.1016/0038-0717(82)90001-3
Burns RG, DeForest JL, Marxsen J, Sinsabaugh RL, Stromberger ME, Wallenstein MD, Weintraub MN, Zoppini A (2013) Soil enzymes in a changing environment: current knowledge and future directions. Soil Biol Biochem 58:216–234. https://doi.org/10.1016/j.soilbio.2012.11.009
Chen J, Wang Q, Li M, Liu F, Li W (2016) Does the different photosynthetic pathway of plants affect soil respiration in a subtropical wetland? Ecol Evol 6:8010–8017. https://doi.org/10.1002/ece3.2523
Cleveland CC, Houlton BZ, Smith WK, Marklein AR, Reed SC, Parton W, Del Grosso SJ, Running SW (2013) Patterns of new versus recycled primary production in the terrestrial biosphere. P Natl Acad Sci USA 110:12733–12737
Cohen D (1994) Modelling the coexistence of annual and perennial plants in temporally varying environments. Plant Spec Biol 9:1–10
Copeland SM, Munson SM, Bradford JB, Butterfield BJ, Gunnell KL (2019) Long-term plant community trajectories suggest divergent responses of native and non-native perennials and annuals to vegetation removal and seeding treatments. Restor Ecol 27:821–831. https://doi.org/10.1111/rec.12928
Cordell D, Drangert J, White S (2009) The story of phosphorus: global food security and food for thought. Global Environ Change 19:292–305. https://doi.org/10.1016/j.gloenvcha.2008.10.009
DeForest JL (2019) Chronic phosphorus enrichment and elevated pH suppresses Quercus spp. leaf litter decomposition in a temperate forest. Soil Biol Biochem 135:206–212. https://doi.org/10.1016/j.soilbio.2019.05.005
DeForest JL, Dorkoski R, Freedman ZB, Smemo KA (2021) Multi-year soil microbial and extracellular phosphorus enzyme response to lime and phosphate addition in temperate hardwood forests. Plant Soil 464:391–404. https://doi.org/10.1007/s11104-021-04947-4
Demmig-Adams B, Adams WW III, Barker DH, Logan BA, Bowling DR, Verhoeven AS (1996) Using chlorophyll fluorescence to assess the fraction of absorbed light allocated to thermal dissipation of excess excitation. Physiol Plant 98:253–264. https://doi.org/10.1034/j.1399-3054.1996.980206.x
Díaz S, Lavorel S, McIntyre S, Falczyk V, Casanoves F, Milchunas DG, Skarpe C, Rusch G, Sternberg M, Noy-Meir I, Landsberg J, Zhang W, Clark H, Campbell BD (2006) Plant trait responses to grazing – a global synthesis. Global Change Biol 13:313–341. https://doi.org/10.1111/j.1442-1984.1994.tb00075.x
Du E, Terrer C, Pellegrini AFA, Ahlström A, van Lissa CJ, Zhao X, Xia N, Wu X, 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
Fargašová A (1996) Inhibitive effect of organotin compounds on the chlorophyll content of the green freshwater alga Scenedesmus quadricauda. Bull Environ Contam Toxicol 57:99–106. https://doi.org/10.1007/s001289900161
Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90. https://doi.org/10.1007/bf00386231
Feng J, Zhu B (2019) A global meta-analysis of soil respiration and its components in response to phosphorus addition. Soil Biol Biochem 135:38–47. https://doi.org/10.1016/j.soilbio.2019.04.008
Fiorentini M, Zenobi S, Giorgini E, Basili D, Conti C, Pro C, Monaci E, Orsini R (2019) Nitrogen and chlorophyll status determination in durum wheat as influenced by fertilization and soil management: preliminary results. PLoS ONE 14:e0225126. https://doi.org/10.1371/journal.pone.0225126
Fornara DA, Tilman D (2009) Ecological mechanisms associated with the positive diversity—productivity relationship in an N-limited grassland. Ecology 90:408–418. https://doi.org/10.1890/08-0325.1
Freschet GT, Roumet C, Comas LH, Weemstra M, Bengough AG, Rewald B, Bardgett RD, De Deyn GB, Johnson D, Klimešová J (2020) Root traits as drivers of plant and ecosystem functioning: current understanding, pitfalls and future research needs. New Phytol 232:1123–1158. https://doi.org/10.1111/nph.17072
García-Palacios P, Gross N, Gaitán J, Maestre FT (2018) Climate mediates the biodiversity–ecosystem stability relationship globally. Proc Natl Acad Sci USA 115:8400–8405. https://doi.org/10.1073/pnas.1800425115
Garlick K, Drew RE, Rajaniemi TK (2021) Root responses to neighbors depend on neighbor identity and resource distribution. Plant Soil 467:227–237. https://doi.org/10.1007/s11104-021-05083-9
Ghannoum O, Conroy JP (2007) Phosphorus deficiency inhibits growth in parallel with photosynthesis in a C3 (Panicum laxum) but not two C4 (P. coloratum and Cenchrus ciliaris) grasses. Funct Plant Biol 34:72–81. https://doi.org/10.1071/FP06253
Ghannoum O, Paul MJ, Ward JL, Beale MH, Corol DI, Conroy JP (2008) The sensitivity of photosynthesis to phosphorus deficiency differs between C3 and C4 tropical grasses. Funct Plant Biol 35:213–221. https://doi.org/10.1071/fp07256
Gong S, Zhang T, Guo J (2020) Warming and nitrogen deposition accelerate soil phosphorus cycling in a temperate meadow ecosystem. Soil Res 58:109–115. https://doi.org/10.1071/sr19114
Graux AI, Resmond R, Casellas E, Delaby L, Faverdin P, Le Bas C, Ripoche D, Ruget F, Thérond O, Vertès F, Peyraud JL (2020) High-resolution assessment of French grassland dry matter and nitrogen yields. Eur J Agron 112:125952. https://doi.org/10.1016/j.eja.2019.125952
Guerrieri R, Belmecheri S, Ollinger SV, Asbjornsen H, Jennings K, Xiao J, Stocker BD, Martin M, Hollinger DY, Bracho-Garrillo R, Clark K, Dore S, Kolb T, Munger JW, Novick K, Richardson AD (2019) Disentangling the role of photosynthesis and stomatal conductance on rising forest water-use efficiency. Proc Natl Acad Sci 16:16909–16914. https://doi.org/10.1073/pnas.1905912116
Güsewell S (2004) N:P ratios in terrestrial plants: variation and functional significance. New Phytol 164:243–266. https://doi.org/10.2307/1514768
Happonen K, Virkkala AM, Kemppinen J, Niittynen P, Luoto M (2022) Relationships between aboveground plant traits and carbon cycling in tundra plant communities. J Ecol 110:700–716. https://doi.org/10.1111/1365-2745.13832
Harpole WS, Suding KN (2011) A test of the niche dimension hypothesis in an arid annual grassland. Oecologia 166:197–205. https://doi.org/10.2307/41499822
Hata K, Osawa T, Hiradate S, Kachi N (2018) Soil erosion alters soil chemical properties and limits grassland plant establishment on an oceanic island even after goat eradication. Restor Ecol 27:333–342. https://doi.org/10.1111/rec.12854
Hayes P, Turner BL, Lambers H, Laliberté E (2014) Foliar nutrient concentrations and resorption efficiency in plants of contrasting nutrient-acquisition strategies along a 2-million-year dune chronosequence. J Ecol 102:396–410. https://doi.org/10.1111/1365-2745.12196
He M, Dijkstra FA (2015) Phosphorus addition enhances loss of nitrogen in a phosphorus-poor soil. Soil Biol Biochem 82:99–106. https://doi.org/10.1016/j.soilbio.2014.12.015
Heuck C, Weig A, Spohn M (2015) Soil microbial biomass C:N:P stoichiometry and microbial use of organic phosphorus. Soil Biol Biochem 85:119–129. https://doi.org/10.1016/j.soilbio.2015.02.029
Higgins SI, O’Hara RB, Römermann C (2012) A niche for biology in species distribution models. J Biogeogr 39:2091–2095. https://doi.org/10.1111/jbi.12029
Holt RD (2009) Bringing the Hutchinsonian niche into the 21st century: ecological and evolutionary perspectives. Proc Natl Acad Sci USA 106:19659–19665. https://doi.org/10.2307/25593251
Huang ZQ, Ran SS, Fu YR, Wan XH, Song X, Chen YX, Yu ZP (2022) Functionally dissimilar neighbors increase tree water use efficiency through enhancement of leaf phosphorus concentration. J Appl Ecol 58:2833–2842. https://doi.org/10.1111/1365-2745.13941
Jacoby RP, Kopriva S (2019) Metabolic niches in the rhizosphere microbiome: new tools and approaches to analyse metabolic mechanisms of plant–microbe nutrient exchange. J Exp Bot 70:1087–1094. https://doi.org/10.1093/jxb/ery438
Kidd DR, Ryan MH, Hahne D, Haling RE, Lambers H, Sandral GA, Simpson R, Cawthray G (2018) The carboxylate composition of rhizosheath and root exudates from twelve species of grassland and crop legumes with special reference to the occurrence of citramalate. Plant Soil 424:389–403. https://doi.org/10.1007/s11104-017-3534-0
Kramer-Walter KR, Bellingham PJ, Millar TR, Smissen RD, Richardson SJ, Laughlin DC (2016) Root traits are multidimensional: specific root length is independent from root tissue density and the plant economic spectrum. J Ecol 104:1299–1310. https://doi.org/10.1111/1365-2745.12562
Krüger GHJ, Jordaan A, Tiedt LR, Strasser RJ, Kilbourn Louw M, Berner JM (2017) Opportunistic survival strategy of Welwitschia mirabilis: recent anatomical and ecophysiological studies elucidating stomatal behaviour and photosynthetic potential. Botany 95:1109–1123. https://doi.org/10.1139/cjb-2017-0095
Lejeune KD, Suding KN, Seastedt TR (2006) Nutrient availability does not explain invasion and dominance of a mixed grass prairie by the exotic forb Centaurea diffusa Lam. Appl Soil Ecol 32:98–110. https://doi.org/10.1016/j.apsoil.2005.01.009
Levey M, Timm S, Mettler-Altmann T, Borghi GL, Koczor M, Arrivault S, Weber APM, Bauwe H, Gowik U, Westhoff P (2018) Efficient 2-phosphoglycolate degradation is required to maintain carbon assimilation and allocation in the C4 plant Flaveria bidentis J Exp Bot 70:575–587. https://doi.org/10.1093/jxb/ery370
Li L, Li SM, Sun JH, Zhou LL, Bao XG, Zhang HG, Zhang FS (2007) Diversity enhances agricultural productivity via rhizosphere phosphorus facilitation on phosphorus-deficient soils. Proc Natl Acad Sci USA 104:11192–11196. https://doi.org/10.1073/pnas.0704591104
Li SX, Wang ZH, Malhi SS, Li SQ, Gao YJ, Tian XH (2009) Nutrient and water management effects on crop production, and nutrient and water use efficiency in dryland areas of China. Adv Agro 102:223–265. https://doi.org/10.1016/S0065-2113(09)01007-4
Li LJ, Zeng DH, Mao R, Yu ZY (2012) Nitrogen and phosphorus resorption of Artemisia scoparia, Chenopodium acuminatum, Cannabis sativa, and Phragmites communis under nitrogen and phosphorus additions in a semiarid grassland, China. Plant Soil Environ 58:446–451. https://doi.org/10.17221/6339-PSE
Li L, Yang H, Peng L, Ren W, Gong J, Liu P, Wu X, Huang F (2019) Comparative study reveals insights of sheepgrass (Leymus Chinensis) coping with phosphate-deprived stress condition. Front Plant Sci 10:170. https://doi.org/10.3389/fpls.2019.00170
Li Z, Liang M, Li Z, Mariotte P, Tong X, Zhang J, Dong L, Zheng Y, Ma W, Zhao L, Wang L, Wen L, Tuvshintogtokh I, Gornish ES, Dang Z, Liang C, Li FY (2021) Plant functional groups mediate effects of climate and soil factors on species richness and community biomass in grasslands of Mongolian Plateau. J Plant Ecol 14:679–691. https://doi.org/10.1093/jpe/rtab021
Lie Z, Zhou G, Huang W, Kadowaki K, Tissue DT, Yan J, Peñuelas J, Sardans J, Li Y, Liu S, Chu G, Meng Z, He X, Liu J (2022) Warming drives sustained plant phosphorus demand in a humid tropical forest. Global Change Biol 28:4085–4096. https://doi.org/10.1111/gcb.16194
Liu M, Zhang Z, He Q, Wang H, Li X, Schoer J (2014) Exogenous phosphorus inputs alter complexity of soil-dissolved organic carbon in agricultural riparian wetlands. Chemosphere 95:572–580. https://doi.org/10.1016/j.chemosphere.2013.09.117
Liu C, Liu Y, Guo K, Qiao X, Zhao H, Wang S, Zhang L, Cai X (2018) Effects of nitrogen, phosphorus and potassium addition on the productivity of a karst grassland: plant functional group and community perspectives. Ecol Eng 117:84–95. https://doi.org/10.1016/j.ecoleng.2018.04.008
Luo Q, Gong J, Yang L, Li X, Pan Y, Liu M, Zhai Z, Baoyin T (2017) Impacts of nitrogen addition on the carbon balance in a temperate semiarid grassland ecosystem. Biol Fert Soils 53:911–927. https://doi.org/10.1007/s00374-017-1233-x
Luo R, Kuzyakov Y, Zhu B, Qiang W, Zhang Y, Pang X (2022) Phosphorus addition decreases plant lignin but increases microbial necromass contribution to soil organic carbon in a subalpine forest. Global Change Biol 13:28. https://doi.org/10.1111/gcb.16205
Lynch J, Brown K (2008) Root strategies for phosphorus acquisition. In: White P, Hammond J (eds) The ecophysiology of plant-phosphorus interaction, vol 7. Springer, Berlin, pp 83–116. https://doi.org/10.1007/978-1-4020-8435-5_5
Lynch JP, Ho MD (2005) Rhizoeconomics: carbon costs of phosphorus acquisition. Plant Soil 269:45–56. https://doi.org/10.1007/s11104-004-1096-4
Ma Z, Guo D, Xu X, Lu M, Bardgett R, Eissenstat DM, McCormack ML, Hedin LO (2018) Evolutionary history resolves global organization of root functional traits. Nature 555:94–97. https://doi.org/10.1038/nature26163
Martini D, Pacheco-Labrador J, Perez-Priego O, Migliavacca M (2019) Nitrogen and phosphorus effect on sun-induced fluorescence and gross primary productivity in Mediterranean grassland. Remote Sens-Basel 11:2562. https://doi.org/10.3390/rs11212562
Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668. https://doi.org/10.1093/jexbot/51.345.659
Mo Q, Li ZA, Sayer EJ, Lambers H, Li Y, Zou B, Tang J, Heskel M, Ding Y, Wang F, Ostertag R (2019) Foliar phosphorus fractions reveal how tropical plants maintain photosynthetic rates despite low soil phosphorus availability. Funct Ecol 33:503–513. https://doi.org/10.1111/1365-2435.13252
Moran R, Wong I, Rodríguez F, Somonte D, de la Torre D, Dominguez L, Valdivia AN, Alvarez I, González N, Paneque Y, Heredia CEP, Mora N, Sánchez I, Rodríguez RF, Galdós L, Verdecia-Mogena A (2017) From the rhizosphere to a bioproduct. The role of plant–microbe interactions. In: 11th International Congress on Plant Biotechnology and Agriculture BIOVEG. https://www.researchgate.net/publication/318147336_From_the_rhizosphere_to_a_bioproduct_The_role_of_plant-microbe_interactions. Accessed May 2017
Onoda Y, Hikosaka K, Hirose T (2004) Allocation of nitrogen to cell walls decreases photosynthetic nitrogen-use efficiency. Funct Ecol 18:419–425. https://doi.org/10.2307/3599203
Pang J, Bansal R, Zhao H, Bohuon E, Lambers H, Ryan MH, Ranathunge K, Siddique KMH (2018) The carboxylate-releasing phosphorus-mobilising strategy could be proxied by foliar manganese concentration in a large set of chickpea germplasm under low phosphorus supply. New Phytol 219:518–529. https://doi.org/10.1111/nph.15200
Pathak KV, Nallapeta S (2014) Plant–microbial interaction: a dialogue between two dynamic bioentities. In: Kavi KPB, Rajib B, Prashanth S (eds) Agricultural bioinformatics. Springer, Berlin, pp 259–272. https://doi.org/10.1007/978-81-322-1880-7_15
Peng ZY, Wu YT, Guo LL, Yang L, Wang B, Wang X, Liu WX, Su YJ, Wu J, Liu LL (2023) Foliar nutrient resorption stoichiometry and microbial phosphatase catalytic efficiency together alleviate the relative phosphorus limitation in forest ecosystems. New Phytol 238:1033–1044. https://doi.org/10.1111/nph.18797
Phoenix GK, Johnson DA, Muddimer SP, Leake JR, Cameron DD (2020) Niche differentiation and plasticity in soil phosphorus acquisition among co-occurring plants. Nat Plants 6:349–354. https://doi.org/10.1038/s41477-020-0624-4
Pianka ER (1973) The structure of lizard communities. Annu Rev Ecol Evol Syst 4:53–74. https://doi.org/10.1146/annurev.es.04.110173.000413
Qaswar M, Li D, Huang J, Han T, Ahmed W, Abbas M, Zhang L, Du J, Khan ZH, Ullah S, Zhang H, Wang B (2020) Interaction of liming and long-term fertilization increased crop yield and phosphorus use efficiency (PUE) through mediating exchangeable cations in acidic soil under wheat–maize cropping system. Sci Rep-UK 10:19828. https://doi.org/10.1038/s41598-020-76892-8
Raiesi F, Beheshti A (2014) Soil specific enzyme activity shows more clearly soil responses to paddy rice cultivation than absolute enzyme activity in primary forests of northwest Iran. Appl Soil Ecol 75:63–70. https://doi.org/10.1016/j.apsoil.2013.10.012
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.1469-8137.2012.04249.x
Reich PB, Wright IJ, Cavender-Bares JC, Craine M, Oleksyn J, Walters MB (2003) The evolution of plant functional variation: traits, spectra, and strategies. Int J Plant Sci 164:S143–S164. https://doi.org/10.1086/374368
Rejmánková E, Sirová D (2007) Wetland macrophyte decomposition under different nutrient conditions: relationships between decomposition rate, enzyme activities and microbial biomass. Soil Biol Biochem 39:526–538. https://doi.org/10.1016/j.soilbio.2006.08.022
Ren F, Song W, Chen L, Mi Z, Zhang Z, Zhu W, Zhou H, Cao G, He JS (2016) Phosphorus does not alleviate the negative effect of nitrogen enrichment on legume performance in an alpine grassland. J Plant Ecol 10:822–830. https://doi.org/10.1093/jpe/rtw089
Richardson AE, Lynch JP, Ryan PR, Delhaize E, Smith FA, Smith SE, Harvey PR, Ryan MH, Veneklaas EJ, Lambers H, Oberson A, Culvenor RA, Simpson RJ (2011) Plant and microbial strategies to improve the phosphorus efficiency of agriculture. Plant Soil 349:121–156
Sanaei A, Ali A (2019) What is the role of perennial plants in semi-steppe rangelands? Direct and indirect effects of perennial on annual plant species. Ecol Indic 98:389–396. https://doi.org/10.1016/j.ecolind.2018.11.012
Shi B, Ling X, Cui H, Song W, Gao Y, Sun W (2020) Response of nutrient resorption of Leymus chinensis to nitrogen and phosphorus addition in a meadow steppe of northeast China. Plant Biol 22:1123–1132. https://doi.org/10.1111/plb.13153
Shi J, Gong J, Baoyin T, Luo Q, Zhai Z, Zhu C, Yang B, Wang B, Zhang Z, Li X (2021) Short-term phosphorus addition increases soil respiration by promoting gross ecosystem production and litter decomposition in a typical temperate grassland in northern China. Catena 197:104952. https://doi.org/10.1016/j.catena.2020.104952
Shi JY, Gong JR, Li XB, Zhang ZH, Zhang WY, Li Y, Song LY, Zhang SQ, Dong JJ, Baoyin TT (2023) Phosphorus application promotedthe sequestration of orthophosphate within soil microorganisms and regulatedthe soil solution P supply in a temperate grassland in northern China: a 31P NMR study. Soil Tillage Res 227:105612. https://doi.org/10.1016/j.still.2022.105612
Shipley B (2006) Net assimilation rate, specific leaf area and leaf mass ratio: which is most closely correlated with relative growth rate? A meta-analysis. Funct Ecol 20:565–574. https://doi.org/10.1111/j.1365-2435.2006.01135.x
Silvertown J (2004) Plant coexistence and the niche. Trends Ecol Evol 19:605–611. https://doi.org/10.1016/j.tree.2004.09.003
Simpson EH (1949) Measurement of diversity. Nature 163:688
Slot M, Winter K (2017) In situ temperature relationships of biochemical and stomatal controls of photosynthesis in four lowland tropical tree species. Plant Cell Environ 40:3055–3068. https://doi.org/10.1111/pce.13071
Smith S (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu Rev Plant Biol 62:227–250. https://doi.org/10.1146/annurev-arplant-042110-103846
Smith B (2022) Declining global leaf nitrogen content: smart resource use by flexible plants? New Phytol 235:1683–1685. https://doi.org/10.1111/nph.18354
Spohn M, Kuzyakov Y (2013) Phosphorus mineralization can be driven by microbial need for carbon. Soil Biol Biochem 61:69–75. https://doi.org/10.1016/j.soilbio.2013.02.013
Spohn M, Ermak A, Kuzyakov Y (2013) Microbial gross organic phosphorus mineralization can be stimulated by root exudates–a P isotopic dilution study. Soil Biol Biochem 65:254–263. https://doi.org/10.1016/j.soilbio.2013.05.028
Strickland MS, Rousk J (2010) Considering fungal:bacterial dominance in soils – methods, controls, and ecosystem implications. Soil Biol Biochem 42:1385–1395. https://doi.org/10.1016/j.soilbio.2010.05.007
Su Y, Ma X, Le J, Li K, Han W, Liu X (2021) Decoupling of nitrogen and phosphorus in dominant grass species in response to long-term nitrogen addition in an alpine grassland in Central Asia. Plant Ecol 222:1–14. https://doi.org/10.1007/s11258-020-01103-3
Sullivan BW, Alvarez-Clare S, Castle SC, Porder S, Reed SC, Schreeg L, Townsend AR, Cleveland CC (2014) Assessing nutrient limitation in complex forested ecosystems: alternatives to large-scale fertilization experiments. Ecology 95:668–681. https://doi.org/10.1890/13-0825.1
Sun Q, Yamada T, Han Y, Takano T (2021) Influence of salt stress on C4 photosynthesis in Miscanthus sinensis Anderss. Plant Biol 23:44–56. https://doi.org/10.1111/plb.13192
Tang ZS, An H, Shangguan ZP (2015) The impact of desertification on carbon and nitrogen storage in the desert steppe ecosystem. Ecol Eng 84:92–99. https://doi.org/10.1016/j.ecoleng.2015.07.023
Tran CTK, Watts-Williams SJ, Smernik RJ, Cavagnaro TR (2020) Effects of plant roots and arbuscular mycorrhizas on soil phosphorus leaching. Sci Total Environ 722:137384. https://doi.org/10.1016/j.scitotenv.2020.137847
Turner BL, Brenes-Arguedas T, Condit R (2018) Pervasive phosphorus limitation of tree species but not communities in tropical forests. Nature 555:367–370. https://doi.org/10.1038/nature25789
van der Sande MT, Arets EJMM, Peña-Claros M, Hoosbeek MR, Cáceres-Siani Y, van der Hout P, Poorter L (2017) Soil fertility and species traits, but not diversity, drive productivity and biomass stocks in a Guyanese tropical rainforest. Funct Ecol 32(2):461–474. https://doi.org/10.1111/1365-2435.12968
Vance ED (1987) An extracted method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707. https://doi.org/10.1016/0038-0717(87)90052-6
Ven A, Verlinden MS, Verbrugge NE, Vicca S (2019) Experimental evidence that phosphorus fertilization and arbuscular mycorrhizal symbiosis can reduce the carbon cost of phosphorus uptake. Funct Ecol 33:1–11. https://doi.org/10.1111/1365-2435.13452
Walk TC, Jaramillo R, Lynch JP (2006) Architectural tradeoffs between adventitious and basal roots for phosphorus acquisition. Plant Soil 279:347–366. https://doi.org/10.2307/24125291
Wang J, Wu Y, Zhou J, Bing H, Sun H (2016) Carbon demand drives microbial mineralization of organic phosphorus during the early stage of soil development. Biol Fert Soils 52:825–839. https://doi.org/10.1007/s00374-016-1123-7
Wang JH, Cai YF, Li SF, Zhang SB (2020) Photosynthetic acclimation of rhododendrons to light intensity in relation to leaf water-related traits. Plant Ecol 221:407–420. https://doi.org/10.1007/s11258-020-01019-y
Warren CR, Adams MA, Chen ZL (2000) Is photosynthesis related to concentrations of nitrogen and rubisco in leaves of Australian native plants? Funct Plant Biol 27:407–416. https://doi.org/10.1071/PP98162
Wassen MJ, Schrader J, van Dijk J, Eppinga MB (2021) Phosphorus fertilization is eradicating the niche of northern Eurasia’ s threatened plant species. Nat Ecol Evol 5:1–7. https://doi.org/10.1038/s41559-020-01323-w
Wen Z, Li H, Shen Q, Tang X, Xiong C, Li H, Pang J, Ryan MH, Lambers H, Shen J (2019) Trade-offs among root morphology, exudation and mycorrhizal symbioses for phosphorus-acquisition strategies of 16 crop species. New Phytol 223:882–895. https://doi.org/10.1111/nph.15833
Wen Z, White PJ, Shen J, Lambers H (2021) Linking root exudation to belowground economic traits for resource acquisition. New Phytol 233:1620–1635. https://doi.org/10.1111/nph.17854
Wijesinghe DK, John EA, Hutchings MJ (2005) Does pattern of soil resource heterogeneity determine plant community structure? An experimental investigation. J Ecol 93:99–112. https://doi.org/10.1111/j.0022-0477.2004.00934.x
Wright IJ, Reich PB, Cornelissen JHC, Falster DS, Garnier E, Hikosaka K, Lamont BB, Lee W, Oleksyn J, Osada N, Poorter H, Villar R, Warton DI, Westoby M (2005) Assessing the generality of global leaf trait relationships. New Phytol 166:485–496. https://doi.org/10.1111/j.1469-8137.2005.01349.x
Xiao L, Liu G, Li P, Li Q, Xue S (2020) Ecoenzymatic stoichiometry and microbial nutrient limitation during secondary succession of natural grassland on the Loess Plateau, China. Soil Tillage Res 200:104605. https://doi.org/10.1016/j.still.2020.104605
Xu B, Yang XC, Tao WG, Miao JM, Yang Z, Liu HQ, Jin YX, Zhu XH, Qin ZH, Lv HY, Li JY (2013) MODIS-based remote-sensing monitoring of the spatiotemporal patterns of China’s grassland vegetation growth. Int J Remote Sens 34:3867–3878. https://doi.org/10.1080/01431161.2012.762696
Yan N, Wang XQ, Xu XF, Guo DP, Wang ZD, Zhang JZ, Hyde KD, Liu HL (2013) Plant growth and photosynthetic performance of Zizania latifolia are altered by endophytic Ustilago esculenta infection. Physiol Mol Plant Pathol 83:75–83. https://doi.org/10.1016/j.pmpp.2013.05.005
Yang H (2018) Effects of nitrogen and phosphorus addition on leaf nutrient characteristics in a subtropical forest. Trees 32:383–391. https://doi.org/10.1007/s00468-017-1636-1
Ye ZP (2007) A new model for relationship between irradiance and the rate of photosynthesis in Oryza sativa Photosynthetica 45:637–640. https://doi.org/10.1007/s11099-007-0110-5
Yin X, Struik PC (2011) C3 and C4 photosynthesis models: an overview from the perspective of crop modelling. NJAS-Wagen J Life Sci 57:27–38. https://doi.org/10.1016/j.njas.2009.07.001
Yu RP, Li XX, Xiao ZH, Lambers H, Li L (2020) Phosphorus facilitation and covariation of root traits in steppe species. New Phytol 226:1285–1298. https://doi.org/10.1111/nph.16499
Zhang D, Zhang C, Tang X, Li H, Zhang F, Rengel Z, Whalley WR, Davies WJ, Shen J (2016) Increased soil phosphorus availability induced by faba bean root exudation stimulates root growth and phosphorus uptake in neighbouring maize. New Phytol 209:823–831. https://doi.org/10.1111/nph.13613
Zhou R, Yu X, Kjær KH, Rosenqvist E, Ottosen CO, Wu Z (2015) Screening and validation of tomato genotypes under heat stress using Fv/Fm to reveal the physiological mechanism of heat tolerance. Environ Exp Bot 118:1–11. https://doi.org/10.1016/j.envexpbot.2015.05.006
Zhou T, Wang L, Sun X, Wang X, Chen Y, Rengel Z, Liu W, Yang W (2019) Light intensity influence maize adaptation to low P stress by altering root morphology. Plant Soil 447:183–197. https://doi.org/10.1007/s11104-019-04259-8
Zhou M, Guo Y, Sheng J, Yuan Y, Zhang WH, Bai W (2022) Using anatomical traits to understand root functions across root orders of herbaceous species in a temperate steppe. New Phytol 234:422–434. https://doi.org/10.1111/nph.17978
Zhu X, Liu M, Kou Y, Liu D, Liu Q, Zhang Z, Jiang Z, Yin H (2020) Differential effects of N addition on the stoichiometry of microbes and extracellular enzymes in the rhizosphere and bulk soils of an alpine shrubland. Plant Soil 449:285–301. https://doi.org/10.1007/s11104-020-04468-6
Funding
This work was funded by the National Key R&D Program of China (Grant No. 2022YFF1303404) and National Natural Science Foundation of China (Grant No. 32230065). We are grateful to Inner Mongolia University for providing us with the study site and Laboratory analysis and Testing Center of State Key Laboratory of Earth Surface Processes and Resource Ecology for helping with the fieldwork and experiments.
Author information
Authors and Affiliations
Contributions
Jirui Gong designed the experiment. Weiyuan Zhang, Siqi Zhang, and Xuede Dong performed sample preparation. Weiyuan Zhang performed the laboratory experiments, analyzed the data, drew figures and tables, and wrote the first draft. Jirui Gong and Hans Lambers made a major contribution to the final version. Siqi Zhang, Xuede Dong, Yuxia Hu, Guisen Yang, and Chenyi Yan contributed to the interpretation of the results and writing of the manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors have no relevant financial or non-financial interests to disclose.
Additional information
Responsible Editor: Adamo Domenico Rombolà.
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Below is the link to the electronic supplementary material.
ESM 1
(DOCX 2.22 MB)
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Zhang, W., Gong, J., Zhang, S. et al. Soil phosphorus availability affects niche characteristics of dominant C3 perennial and sub-dominant C4 annual species in a typical temperate grassland of northern China. Plant Soil (2024). https://doi.org/10.1007/s11104-024-06655-1
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11104-024-06655-1