Abstract
Background and aims
Nitrogen (N) and phosphorus (P) availabilities limit plant productivity, especially in primary succession; however, our understanding of species-specific strategies regarding their allocation and coordination with other functional traits remains limited.
Methods
Community-weighted mean traits were compared to decipher the ecophysiological mechanisms of forest succession in nine dominant species along 120-y successional stages across a glacier-retreating chronosequence.
Results
High foliar N and P concentrations in N2-fixing plants on a 12-year-old surface did not result in high photosynthetic capacity due to the inefficient allocation, as indicated by their low photosynthetic N- and P-use efficiencies. On a 40-year-old surface, exploitative strategies, manifested in a higher specific leaf area and greater N allocation to Rubisco, as well as quick-return energy economics, helped deciduous forests dominate. When P availability decreased on a 120-year-old surface, evergreens maintained high photosynthetic P-use efficiency, by reducing overall P concentration and its allocation to structural fraction. Efficient P allocation and a higher ratio of leaf lifespan to payback time facilitated the dominance of evergreens in low P-sites.
Conclusions
Optimizing allocation of limiting N or P among foliar fractions and fast–slow economic strategies drive primary succession after glacier retreat. Integrating the above- and below-ground subsystems through food webs will provide further insights into ecosystem dynamics.
Similar content being viewed by others
References
Acharya K, Kyle M, Elser JJ (2004) Biological stoichiometry of Daphnia growth: An ecophysiological test of the growth rate hypothesis. Limnol Oceanogr 49:656–665. https://doi.org/10.4319/lo.2004.49.3.0656
Adler PB, Fajardo A, Kleinhesselink AR, Kraft NJ (2013) Trait-based tests of coexistence mechanisms. Ecol Lett 16:1294–1306. https://doi.org/10.1111/ele.12157
Allen AP, Gillooly JF (2009) Towards an integration of ecological stoichiometry and the metabolic theory of ecology to better understand nutrient cycling. Ecol Lett 12:369–384. https://doi.org/10.1111/j.1461-0248.2009.01302.x
Atkin OK, Turnbull MH, Zaragoza-Castells J, Fyllas NM, Lloyd J, Meir P, Griffin KL (2013) Light inhibition of leaf respiration as soil fertility declines along a post-glacial chronosequence in New Zealand: An analysis using the Kok method. Plant Soil 367:163–182. https://doi.org/10.1007/s11104-013-1686-0
Bacete L, Melida H, Miedes E, Molina A (2018) Plant cell wall-mediated immunity: cell wall changes trigger disease resistance responses. Plant J 93:614–636. https://doi.org/10.1111/tpj.13807
Bar-On YM, Milo R (2019) The global mass and average rate of rubisco. Proc Natl Acad Sci USA 116:4738–4743. https://doi.org/10.1073/pnas.1816654116
Bernasconi SM, Bauder A, Bourdon B, Brunner I, Bünemann E, Chris I, Derungs N, Edwards P, Farinotti D, Frey B, Frossard E, Furrer G, Gierga M, Goransson H, Gulland K, Hagedorn F, Hajdas I, Hindshaw R, Ivy-Ochs S, Jansa J, Jonas T, Kiczka M, Kretzschmar R, Lemarchand E, Luster J, Magnusson J, Mitchell EAD, Venterink HO, Plotze M, Reynolds B, Smittenberg RH, Stahli M, Tamburini F, Tipper ET, Wacker L, Welc M, Wiederhold JG, Zeyer J, Zimmermann S, Zumsteg A (2011) Chemical and biological gradients along the Damma Glacier soil chronosequence, Switzerland. Vadose Zone J 10:867–883. https://doi.org/10.2136/vzj2010.0129
Buma B, Bisbing S, Krapek J, Wright G (2017) A foundation of ecology rediscovered: 100 years of succession the William S. Cooper plots in Glacier Bay. Alaska Ecology 98:1513–1523. https://doi.org/10.1002/ecy.1848
Caccianiga M, Luzzaro A, Pierce S, Ceriani RM, Cerabolini B (2006) The functional basis of a primary succession resolved by CSR classification. Oikos 112:10–20. https://doi.org/10.1111/j.0030-1299.2006.14107.x
Cavatte PC, Rodriguez-Lopez NF, Martins SCV, Mattos MS, Sanglard LMVP, DaMatta FM (2012) Functional analysis of the relative growth rate, chemical composition, construction and maintenance costs, and the payback time of Coffea arabica L. leaves in response to light and water availability. J Exp Bot 63:3071–3082. https://doi.org/10.1093/jxb/ers027
Chen L, Swenson NG, Ji NN, Mi XC, Ren HB, Guo LD, Ma KP (2019) Differential soil fungus accumulation and density dependence of trees in subtropical forest. Science 366:124–128. https://doi.org/10.1126/science.aau1361
Clements FE (1916) Plant succession: an analysis of the development of vegetation. No. 242. Carnegie Institution of Washington Press of Gibson Brothers, Washington
Cooper WS (1923) The recent ecological history of Glacier Bay, Alaska: permanent quadrats at Glacier Bay: an initial report upon a long-period study. Ecology 4:355–365. https://doi.org/10.2307/1929182
Cooper WS (1931) A third expedition to Glacier Bay, Alaska. Ecology 12:61–95. https://doi.org/10.2307/1932934
Cooper WS (1939) A fourth expedition to Glacier Bay, Alaska. Ecology 20:130–155. https://doi.org/10.2307/1930735
Cowles HC (1901) The physiographic ecology of Chicago and vicinity; a study of the origin, development, and classification of plant societies Contribution from the Hull Botanical Laboratory. Bot Gaz 31:145–182. https://doi.org/10.1086/328080
Darcy JL, Schmidt SK, Knelman JE, Cleveland CC, Castle SC, Nemergut DR (2018) Phosphorus, not nitrogen, limits plants and microbial primary producers following glacial retreat. Sci Adv 4:eaaq0942. https://doi.org/10.1126/sciadv.aaq0942
Delgado M, Valle S, Reyes-Díaz M, Barra PJ, Zúñiga-Feest A (2018) Nutrient use efficiency of southern South America Proteaceae species. Are there general patterns in the Proteaceae family? Front Plant Sci 9:883–895. https://doi.org/10.3389/fpls.2018.00883
Díaz S, Kattge J, Cornelissen JHC, Wright IJ, Lavorel S, Dray S, Reu B, Kleyer M, Wirth C, Prentice IC, Garnier E, Bonisch G, Westoby M, Poorter H, Reich PB, Moles AT, Dickie J, Gillison A,N, Zanne AE, Chave J, Wright SJ, Sheremet’ev SN, Jactel H, Baraloto C, Cerabolini B, Pierce S, Shipley B, Kirkup D, Casanoves F, Joswig JS, Gunther A, Falczuk V, Ruger N, Mahecha MD, Gorne LD (2016) The global spectrum of plant form and function. Nature 529:167–173. https://doi.org/10.1038/nature16489
Du EZ, Terrer C, Pellegrini AFA, Ahlstrom 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
Egler FE (1954) Vegetation science concepts. I. Initial floristic composition, a factor in old-field vegetation development. Vegetatio 4:412–417. https://doi.org/10.1007/BF00275587
Fastie CL (1995) Causes and ecosystem consequences of multiple pathways of primary succession at Glacier Bay, Alaska. Ecology 76:1899–1916. https://doi.org/10.2307/1940722
Hayes PE, Clode PL, Oliveira RS, Lambers H (2018) Proteaceae from phosphorus-impoverished habitats preferentially allocate phosphorus to photosynthetic cells: An adaptation improving phosphorus-use efficiency. Plant Cell Environ 41:605–619. https://doi.org/10.1111/pce.13124
Hidaka A, Kitayama K (2009) Divergent patterns of photosynthetic phosphorus-use efficiency versus nitrogen-use efficiency of tree leaves along nutrient-availability gradients. J Ecol 97:984–991. https://doi.org/10.1111/j.1365-2745.2009.01540.x
Hidaka A, Kitayama K (2011) Allocation of foliar phosphorus fractions and leaf traits of tropical tree species in response to decreased soil phosphorus availability on Mount Kinabalu, Borneo. J Ecol 99:849–857. https://doi.org/10.1111/j.1365-2745.2011.01805.x
Hou EQ, Luo YQ, Kuang YW, Chen CR, Lu XK, Jiang LF, Luo XZ, Wen DZ (2020) Global meta-analysis shows pervasive phosphorus limitation of aboveground plant production in natural terrestrial ecosystems. Nat Commun 11:637. https://doi.org/10.1038/s41467-020-14492-w
Idso KE, Hoober JK, Idso SB, Wall GW, Kimball BA (2001) Atmospheric CO2 enrichment influences the synthesis and mobilization of putative vacuolar storage proteins in sour orange tree leaves. Environ Exp Bot 48:199–211. https://doi.org/10.1016/S0098-8472(02)00017-5
Jiang YL, Lei YB, Yang Y, Korpelainen H, Niinemets Ü, Li CY (2018a) Divergent assemblage patterns and driving forces for bacterial and fungal communities along a glacier forefield chronosequence. Soil Biol Biochem 118:207–216. https://doi.org/10.1016/j.soilbio.2017.12.019
Jiang YL, Song MY, Zhang S, Cai ZQ, Lei YB (2018b) Unravelling community assemblages through multi-element stoichiometry in plant leaves and roots across primary successional stages in a glacier retreat area. Plant Soil 428:291–305. https://doi.org/10.1007/s11104-018-3683-9
Jonard M, Furst A, Verstraeten A, Thimonier A, Timmermann V, Potocic N, Waldner P, Benham S, Hansen K, Merila P, Ponette Q, de la Cruz AC, Roskams P, Nicolas M, Croise L, Ingerslev M, Matteucci G, Decinti B, Bascietto M, Rautio P (2015) Tree mineral nutrition is deteriorating in Europe. Glob Change Biol 21:418–430. https://doi.org/10.1111/gcb.12657
Kedrowski RA (1983) Extraction and analysis of nitrogen, phosphorus and carbon fractions in plant material. J Plant Nutr 6:989–1011. https://doi.org/10.1080/01904168309363161
Klauer SF, Franceschi VR, Ku MSB, Zhang DZ (1996) Identification and localization of vegetative storage proteins in legume leaves. Am J Bot 83:1–10. https://doi.org/10.2307/2445947
Knelman JE, Legg TM, O’Neill SP, Washenberger CL, González A, Cleveland CC, Nemergut DR (2012) Bacterial community structure and function change in association with colonizer plants during early primary succession in a glacier forefield. Soil Biol Biochem 46:172–180. https://doi.org/10.1016/j.soilbio.2011.12.001
Kornfeld A, Atkin OK, Griffin KL, Horton TW, Yakir D, Turnbull MH (2013) Modulation of respiratory metabolism in response to nutrient changes along a soil chronosequence. Plant Cell Environ 36:1120–1134. https://doi.org/10.1111/pce.12047
Lambers H, Cawthray GR, Giavalisco P, Kuo J, Laliberté E, Pearse SJ, Scheible WR, Stitt M, Teste F, Turner BL (2012) Proteaceae from severely phosphorus-impoverished soils extensively replace phospholipids with galactolipids and sulfolipids during leaf development to achieve a high photosynthetic phosphorus-use-efficiency. New Phytol 196:1098–1108. https://doi.org/10.1111/j.1469-8137.2012.04285.x
Lamport DTA (1965) The protein component of primary cell walls. Adv Bot Res 2:151–218. https://doi.org/10.1016/S0065-2296(08)60251-7
Laungani R, Knops JMH (2009) Species-driven changes in nitrogen cycling can provide a mechanism for plant invasions. Proc Natl Acad Sci USA 106:12400–12405. https://doi.org/10.1073/pnas.0900921106
Lei YB, Zhou J, Xiao HF, Duan BL, Wu YH, Korpelainen H, Li CY (2015) Soil nematode assemblages as bioindicators of primary succession along a 120-year-old chronosequence on the Hailuogou Glacier forefield, SW China. Soil Biol Biochem 88:362–371. https://doi.org/10.1016/j.soilbio.2015.06.013
Lei YB, Jiang YL, Chen K, Duan BL, Zhang S, Korpelainen H, Niinemets Ü, Li CY (2017) Reproductive investments driven by sex and altitude in sympatric Populus and Salix trees. Tree Physiol 37:1503–1514. https://doi.org/10.1093/treephys/tpx075
Li X, Xiong SF (1995) Vegetation primary succession on glacier foreland in Hailuogou Mt Gongga. Mt Res 13:109–115 ((in Chinese with English abstract))
Lovelock CE, Reef R, Pandolf JM (2014) Variation in elemental stoichiometry and RNA: DNA in four phyla of benthic organisms from coral reefs. Funct Ecol 28:1299–1309. https://doi.org/10.1111/1365-2435.12256
Matzek V, Vitousek PM (2009) N: P stoichiometry and protein: RNA ratios in vascular plants: an evaluation of the growth-rate hypothesis. Ecol Lett 12:765–771. https://doi.org/10.1111/j.1461-0248.2009.01310.x
McQuillan M, Smernik RJ, Doolette AL (2020) Partitioning of phosphorus between biochemical and storage compounds in leaves follows a consistent pattern across four Australian genera growing in native settings. Plant Soil 454:57–75. https://doi.org/10.1007/s11104-020-04567-4
Navas ML, Ducout B, Roumet C, Richarte J, Garnier J, Garnier E (2003) Leaf life span, dynamics and construction cost of species from Mediterranean old-fields differing in successional status. New Phytol 159: 213–228. https://doi.org/10.1046/j.1469-8137.2003.00790.x
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/10.1111/j.0269-8463.2004.00847.x
Onoda Y, Wright IJ, Evans JR, Hikosaka K, Kitajima K, Niinemets Ü, Poorter H, Tosens T, Westoby M (2017) Physiological and structural tradeoffs underlying the leaf economics spectrum. New Phytol 214:1447–1463. https://doi.org/10.1111/nph.14496
Park M, Kim SJ, Vitale A, Hwang I (2004) Identification of the protein storage vacuole and protein targeting to the vacuole in leaf cells of three plant species. Plant Physiol 134:625–639. https://doi.org/10.1104/pp.103.030635
Parkinson JA, Allen SE (1975) A wet oxidation procedure suitable for the determination of nitrogen and mineral nutrients in biological material. Commun Soil Sci Plant Anal 6:1–11. https://doi.org/10.1080/00103627509366539
Peltzer DA, Wardle DA, Allison VJ, Baisden WT, Bardgett RD, Chadwick OA, Condron LM, Parfitt RL, Porder S, Richardson SJ, Turner BL, Vitousek PM, Walker J, Walker LR (2010) Understanding ecosystem retrogression. Ecol Monogr 80:509–529. https://doi.org/10.1890/09-1552.1
Penuelas J, Poulter B, Sardans J, Ciais P, van der Velde M, Bopp L, Boucher O, Godderis Y, Hinsinger P, Llusia J, Nardin E, Vicca S, Obersteiner M, Janssens IA (2013) Human-induced nitrogen-phosphorus imbalances alter natural and managed ecosystems across the globe. Nat Commun 4:2934. https://doi.org/10.1038/ncomms3934
Pereira CG, Hayes PE, O’Sullivan OS, Weerasinghe LK, Clode PL, Atkin OK, Lambers H (2019) Trait convergence in photosynthetic nutrient-use efficiency along a 2-million year dune chronosequence in a global biodiversity hotspot. J Ecol 107:2006–2023. https://doi.org/10.1111/1365-2754.13158
Poorter H, Pepin S, Rijkers T, De Jong Y, Evans JR, Körner C (2006) Construction costs, chemical composition and payback time of high and low-irradiance leaves. J Exp Bot 57:355–371. https://doi.org/10.1093/jxb/erj002
Prietzel J, Dümig A, Wu Y, Zhou J, Klysubun W (2013) Synchrotron-based P K-edge XANES spectroscopy reveals rapid changes of phosphorus speciation in the topsoil of two glacier foreland chronosequences. Geochimt Cosmochim Acta 108:154–171. https://doi.org/10.1016/j.gca.2013.01.029
Read DJ, Perez-Moreno J (2003) Mycorrhizas and nutrient cycling in ecosystems - a journey towards relevance? New Phytol 157:475–492. https://doi.org/10.1046/j.1469-8137.2003.00704.x
Redfield AC (1958) The biological control of chemical factors in the environment. Am Sci 46:205–221
Reich PB (2014) The world-wide ‘fast-slow’ plant economics spectrum: a traits manifesto. J Ecol 102:275–301. https://doi.org/10.1111/1365-2745.12211
Reich PB, Walters MB, Ellsworth DS (1997) From tropics to tundra: Global convergence in plant functioning. Proc Natl Acad Sci USA 94:13730–13734. https://doi.org/10.1073/pnas.94.25.13730
Reich PB, Ellsworth DS, Walters MB, Vose JM, Gresham C, Volin JC, Bowman WD (1999) Generality of leaf trait relationships: a test across six biomes. Ecology 80:1955–1969. https://doi.org/10.1890/0012-9658(1999)080[1955:GOLTRA]2.0.CO;2
Richardson S, Peltzer D, Allen R, Mcglone M, Parfitt R (2004) Rapid development of phosphorus limitation in temperate rainforest along the Franz Josef soil chronosequence. Oecologia 139:267–276. https://doi.org/10.1007/s00442-004-1501-y
Rime T, Hartmann M, Frey B (2016) Potential sources of microbial colonizers in an initial soil ecosystem after retreat of an alpine glacier. ISME J 10:1625–1641. https://doi.org/10.1038/ismej.2015.238
Schmidt SK, Porazinska D, Concienne BL, Darcy JL, King AJ, Nemergut DR (2016) Biogeochemical stoichiometry reveals P and N limitation across the post-glacial landscape of Denali National Park, Alaska. Ecosystems 19:1164–1177. https://doi.org/10.1007/s10021-016-9992-z
Sulpice R, Ishihara H, Schlereth A, Cawthray GR, Encke B, Giavalisco P, Ivakov A, Arrivault S, Jost R, Krohn N, Kuo J, Laliberte E, Pearse SJ, Raven JA, Scheible WR, Teste F, Veneklaas EJ, Stitt M, Lambers H (2014) Low levels of ribosomal RNA partly account for the very high photosynthetic phosphorus-use efficiency of Proteaceae species. Plant Cell Environ 37:1276–1298. https://doi.org/10.1111/pce.12240
Tang JC, Sun BD, Cheng RM, Shi ZM, Luo D, Liu SR, Centritto M (2019) Seedling leaves allocate lower fractions of nitrogen to photosynthetic apparatus in nitrogen fixing trees than in non-nitrogen fixing trees in subtropical China. PLoS One 14:e0208971. https://doi.org/10.1371/journal.pone.0208971
Turnbull MH, Griffin KL, Fyllas NM, Lloyd J, Meir P, Atkin OK (2016) Separating species and environmental determinants of leaf functional traits in temperate rainforest plants along a soil-development chronosequence. Func Plant Biol 43:751–765. https://doi.org/10.1071/FP16035
Walker LR, del Moral R (2003) Primary Succession and Ecosystem Rehabilitation. Cambridge University Press, Cambridge
Walker TW, Syers JK (1976) The fate of phosphorus during pedogenesis. Geoderma 15:1–19. https://doi.org/10.1016/0016-7061(76)90066-5
Walker LR, Wardle DA, Bardgett RD, Clarkson BD (2010) The use of chronosequences in studies of ecological succession and soil development. J Ecol 98:725–736. https://doi.org/10.1111/j.1365-2745.2010.01664.x
Wang JP, Wu YH, Zhou J, Bing HJ, Sun HY, He QQ, Li JJ, Wilcke W (2020) Soil microbes become a major pool of biological phosphorus during the early stage of soil development with little evidence of competition for phosphorus with plants. Plant Soil 446:259–274. https://doi.org/10.1007/s11104-019-04329-x
Wardle D, Walker L, Bardgett R (2004) Ecosystem properties and forest decline in contrasting long-term chronosequences. Science 305:509–513. https://doi.org/10.1126/science.1098778
Whitehead D, Boelman NT, Turnbull MH, Griffin KL, Tissue DT, Barbour MM, Hunt JE, Richardson SJ, Peltzer DA (2005) Photosynthesis and reflectance indices for rainforest species in ecosystems undergoing progression and retrogression along a soil fertility chronosequence in New Zealand. Oecologia 144:233–244. https://doi.org/10.1007/s00442-005-0068-6
Williams K, Percival F, Merino J, Mooney HA (1987) Estimation of tissue construction cost from heat of combustion and organic nitrogen content. Plant Cell Environ 10:725–734. https://doi.org/10.1111/1365-3040.ep11604754
Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JH, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas ML, Niinemets U, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004) The worldwide leaf economics spectrum. Nature 428:821–827. https://doi.org/10.1038/nature02403
Wu YH, Zhou J, Bing HJ, Sun HY, Wang JP (2015) Rapid loss of phosphorus during early pedogenesis along a glacier retreat chronosequence, Gongga Mountain (SW China). Peer J 3:e1377. https://doi.org/10.7717/peerj.1377
Xiao Y, Liu S, Tong F, Chen B, Kuang Y (2018) Dominant species in subtropical forests could decrease photosynthetic N allocation to carboxylation and bioenergetics and enhance leaf construction costs during forest succession. Front Plant Sci 9:117. https://doi.org/10.3389/fpls.2018.00117
Yang BR, Kallio HP (2001) Fatty acid composition of lipids in sea buckthorn (Hippophae rhamnoides L.) berries of different origins. J Agric Food Chem 49:1939–1947. https://doi.org/10.1021/jf001059s
Yang Y, Wang G, Shen H, Yang Y, Cui H, Liu Q (2014) Dynamics of carbon and nitrogen accumulation and C:N stoichiometry in a deciduous broadleaf forest of deglaciated terrain in the eastern Tibetan plateau. For Ecol Manag 312:10 – 18. https://doi.org/10.1016/j.foreco.2013.10.028
Yang YZ, Wang H, Harrison SP, Prentice IC, Wright IJ, Peng CH, Lin GH (2019) Quantifying leaf-trait covariation and its controls across climates and biomes. New Phytol 221:155–168. https://doi.org/10.1111/nph.15422
Yu L, Song MY, Lei YB, Korpelainen H, Niinemets U, Li CY (2019) Effects of competition and phosphorus fertilization on leaf and root traits of late-successional conifers Abies fabri and Picea brachytyla. Environ Exp Bot 162:14–24. https://doi.org/10.1016/j.envexpbot.2019.02.004
Zhang GH, Zhang LL, Wen DZ (2018) Photosynthesis of subtropical forest species from different successional status in relation to foliar nutrients and phosphorus fractions. Sci Rep 8:10455. https://doi.org/10.1038/s41598-018-28800-4
Zhong XH, Luo J, Wu N (1997) Researches of the forest ecosystems on Gongga Mountain. Chengdu University of Science and Technology Press, Chengdu
Zhou J, Wu Y, Prietzel J, Bing H, Yu D, Sun S, Luo J, Sun H (2013) Changes of soil phosphorus speciation along a 120-year soil chronosequence in the Hailuogou Glacier retreat area (Gongga Mountain, SW China). Geoderma 195–196:251–259. https://doi.org/10.1016/j.geoderma2012.12.010
Acknowledgements
This study was jointly supported by the National Natural Science Foundation of China (31971632), the Second Tibetan Plateau Scientific Expedition and Research Program (2019QZKK0302), the National Key Research and Development Program of China (2020YFE0203200), Sichuan Science & Technology Bureau (2019YFH0042, 2019YFH0132 and 2019YFS0468) and Jiuzhaigou Post-Disaster Restoration and Reconstruction Program. We want to thank Dr Weitao Li, Dr Yonglei Jiang and Mr. Quan Lan for their generous help during plant sampling and data analysis. We also thank Editage (https://www.editage.cn) and Letpub (http://www.letpub.com.cn/) for the linguistic assistance during the preparation of this manuscript.
Author information
Authors and Affiliations
Contributions
Yanbao Lei had the main responsibility for experimental design, data collection, analysis and writing, Liushan Du, and Ke Chen contributed to data collection and analysis, Anđelka Plenković-Moraj contributed to the manuscript preparation, and Geng Sun (the corresponding author) had the overall responsibility for experimental design and project management.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Responsible Editor: Hans Lambers.
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
ESM 1
(DOCX 36.9 KB)
Rights and permissions
About this article
Cite this article
Lei, Y., Du, L., Chen, K. et al. Optimizing foliar allocation of limiting nutrients and fast‐slow economic strategies drive forest succession along a glacier retreating chronosequence in the eastern Tibetan Plateau. Plant Soil 462, 159–174 (2021). https://doi.org/10.1007/s11104-020-04827-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-020-04827-3