Abstract
Leaf stoichiometry and its biogeography play vital roles in nutrient cycling of plant communities. To understand the potential drivers of leaf stoichiometry in karst ecosystems, we measured leaf morphological traits (dry mass content (DM), specific leaf area (SLA)), and biochemical traits (C, N, P, K and Ca stoichiometry) of 53 species of different functional groups, as well as soil properties, across seven karst sites in Southwest China, and explored the relationships between these leaf traits and environmental factors. The results showed that: (1) in karst areas of Southwest China, there were higher leaf C and Ca concentrations as well as higher N/P and K/P ratios compared to other ecosystems, plants were more limited by P rather than by N; (2) mean annual temperature positively influenced leaf N, P, and Ca, while mean annual precipitation exerted more influence on leaf K; (3) a strong phylogeny signal was detected in leaf N (p < 0.05), and significant influence of species composition on the variance of leaf N, K, and Ca was observed (p < 0.05); (4) the influence of soil properties on leaf P and Ca, and the influence of leaf features (SLA and DM) on leaf K were also observed based on a variance partitioning analysis. Abiotic factors such as soil, site, and climate were more important than biotic factors (leaf features and phylogeny) in determining leaf N, P, and Ca. In general, the driving factors exhibited a synergistic effect on leaf stoichiometry across different sites, offering a key mechanism that needs to be integrated into the modeling of biogeochemical nutrients cycling in karst ecosystems.
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27 July 2021
A Correction to this paper has been published: https://doi.org/10.1007/s10533-021-00834-3
References
Asner GP, Martin RE (2016) Convergent elevation trends in canopy chemical traits of tropical forests. Glob Change Biol 22:2216–2227. https://doi.org/10.1111/gcb.13164
Aerts R, Chapin FS III (2000) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Adv Ecol Res 30:1–67. https://doi.org/10.1016/S0065-2504(08)60016-1
Bai K, Lv S, Ning S, Zeng D, Guo Y, Wang B (2019) Leaf nutrient concentrations associated with phylogeny, leaf habit and soil chemistry in tropical karst seasonal rainforest tree species. Plant Soil 434:305–326. https://doi.org/10.1007/s11104-018-3858-4
Bai K, Wei Y, Zhang D, Fu L, Lv S, Deng L (2020) Contrasting effects of light, soil chemistry and phylogeny on leaf nutrient concentrations in cave-dwelling plants. Plant Soil 448:105–120. https://doi.org/10.1007/s11104-020-04422-6
Bao S (2008) Soil and agricultural chemistry analysis, 3rd edn. China Agriculture Press, Beijing (in Chinese)
Blomberg SP, Garland T (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57:717–745. https://doi.org/10.1111/j.0014-3820.2003.tb00285.x
Cao J, Wang X, Adamowski JF, Biswas A, Liu C, Chang Z, Feng Q (2020) Response of leaf stoichiometry of Oxytropis ochrocephala to elevation and slope aspect. CATENA 194:104472. https://doi.org/10.1016/j.catena.2020.104772
Chen Y, Han W, Tang L, Tang Z, Fang J (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
Du Y, Pan G, Li L, Hu Z, Wang X (2011) Leaf N/P ratio and nutrient reuse between dominant species and stands: predicting phosphorus deficiencies in Karst ecosystems, southwestern China. Environ Earth Sci 64:299–309. https://doi.org/10.1007/s12665-010-0847-1
Elser JJ, Fagan WF, Kerkhoff AJ, Swenson NG, Enquist BJ (2010) Biological stoichiometry of plant production: metabolism, scaling and ecological response to global change. New Phytol 186:593–608. https://doi.org/10.1111/j.1469-8137.2010.03214.x
Esmeijer-Liu AJ, Aerts R, Kürschner WM, Bobbink R, Lotter AF, Verhoeven JTA (2009) Nitrogen enrichment lowers Betula pendula green and yellow leaf stoichiometry irrespective of effects of elevated carbon dioxide. Plant Soil 316:311–322. https://doi.org/10.1007/s11104-008-9783-1
Fang H, Yu G, Cheng S, Zhu T, Zheng J, Mo J, Yan J, Luo Y (2011) Nitrogen-15 signals of leaf-litter-soil continuum as a possible indicator of ecosystem nitrogen saturation by forest succession and N loads. Biogeochemistry 102:251–263. https://doi.org/10.1007/s10533-010-9438-1
Fu Z, Chen H, Zhang W, Xu W, Wang S, Wang K (2015) Subsurface flow in a soil-mantled subtropical dolomite karst slope: a field rainfall simulation study. Geomorphology 250:1–14. https://doi.org/10.1016/j.geomorph.2015.08.012
Güsewell S (2004) N:P ratios in terrestrial plants: variation and functional significance. New Phytol 164:243–266. https://doi.org/10.1111/j.1469-8137.2004.01192.x
Han W, Fang J, Guo D, Zhang Y (2005) Leaf nitrogen and phosphorus stoichiometry across 753 terrestrial plant species in China. New Phytol 168(2):377–385. https://doi.org/10.1111/j.1469-8137.2005.01530.x
Han W, Fang J, Reich PB, Woodward FI, Wang Z (2011) Biogeography and variability of eleven mineral elements in plant leaves across gradients of climate, soil and plant functional type in China. Ecol Lett 14:788–796. https://doi.org/10.1111/j.1461-0248.2011.01641.x
Hao Z, Kuang Y, Kang M (2015) Untangling the influence of phylogeny, soil and climate on leaf element concentrations in a biodiversity hotspot. Funct Ecol 29:165–176. https://doi.org/10.1111/1365-2435.12344
Hobbie SE, Gough L (2002) Foliar and soil nutrients in tundra on glacial landscapes of contrasting ages in northern Alaska. Oecologia 131:453–462. https://doi.org/10.1007/s00442-002-0892-x
Holdaway RJ, Richardson SJ, Dickie IA, Peltzer DA, Coomes DA (2011) Species- and community-level patterns in fine root traits along a 120 000-year soil chronosequence in temperate rain forest. J Ecol 99:954–963. https://doi.org/10.1111/j.1365-2745.2011.01821.x
Houlton BZ, Wang YP, Vitousek PM, Field CB (2008) A unifying framework for dinitrogen fixation in the terrestrial biosphere. Nature 454:327–330. https://doi.org/10.1038/nature07028
Huang D, Wang D, Ren Y (2019) Using leaf nutrient stoichiometry as an indicator of flood tolerance and eutrophication in the riparian zone of the Lijang River. Ecol Indic 98:821–829. https://doi.org/10.1016/j.ecolind.2018.11.064
Jiang Z, Lian Y, Qin X (2014) Rocky desertification in Southwest China: Impacts, causes, and restoration. Earth-Sci Rev 132:1–12. https://doi.org/10.1016/j.earscirev.2014.01.005
Jones JB (2001) Laboratory guide for conducting soil tests and plant analysis. CRC Press
Kang H, Zhuang H, Wu L, Liu Q, Shen G, Berg B, Ma R, Liu C (2011) Variation in leaf nitrogen and phosphorus stoichiometry in Picea abies across Europe: an analysis based on local observations. For Eco Manag 261:195–202. https://doi.org/10.1016/j.foreco.2010.10.004
Kamilar JM, Cooper N (2013) Phylogenetic signal in primate behavior, ecology and life history. Philos T R Soc B 368:20120341. https://doi.org/10.1098/rstb.2012.0341
Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464. https://doi.org/10.1093/bioinformatics/btq166
Liu C, Liu Y, Guo K, Wang S, Yang Y (2014) Concentrations and resorption patterns of 13 nutrients in different plant functional types in the karst region of south-western China. Ann Bot Lond 113:873–885. https://doi.org/10.1093/aob/mcu005
Liu J, Fang X, Tang X et al (2019) Patterns and controlling factors of plant nitrogen and phosphorus stoichiometry across China’s forests. Biogeochemistry 143:191–205. https://doi.org/10.1007/s10533-019-00556-7
Liu X, Zhang Y, Han W et al (2013) Enhanced nitrogen deposition over China. Nature 494:459–462. https://doi.org/10.1038/nature11917
Liu X, Zhou G, Zhang D, Liu S, Chu G, Yan J (2010) N and P stoichiometry of plant and soil in lower subtropical forest successional series in southern China. Chin J Plant Ecol 34:64–71 (in Chinese)
Li Y, Mao W, Zhao X, Zhang T (2010) Leaf nitrogen and phosphorus stoichiometry in typical desert and desertified regions, North China. Environ Sci 31(8):1716–1725 (in Chinese)
Lynch JP, St Clair SB (2004) Mineral stress: the missing link in understanding how global climate change will affect plants in real world soils. Field Crop Res 90:101–115. https://doi.org/10.1016/j.fcr.2004.07.008
Manzoni S, Trofymow JA, Jackson RB, Porporato A (2010) Stoichiometric controls on carbon, nitrogen, and phosphorus dynamics in decomposing litter. Ecol Monogr 80:89–106. https://doi.org/10.1890/09-0179.1
Niinemets Ü, Kull K (2005) Co-limitation of plant primary productivity by nitrogen and phosphorus in a species-rich wooded meadow on calcareous soils. Acta Oecol 28:345–356. https://doi.org/10.1016/j.actao.2005.06.003
Ordoñez JC, Bodegom PMV, Jan-Philip MW, Wright IJ, Reich PB, Aerts R (2009) A global study of relationships between leaf traits, climate and soil measures of nutrient fertility. Glob Ecol Biogeogr 18:137–149. https://doi.org/10.1111/j.1466-8238.2008.00441.x
Pan F, Zhang W, Liu S, Li D, Wang K (2015) Leaf N: P stoichiometry across plant functional groups in the karst region of southwestern China. Tress 29:883–892. https://doi.org/10.1007/s00468-015-1170-y
Pang D, Wang G, Li G, Sun Y, Liu Y, Zhou J (2018) Ecological stoichiometric characteristics of two typical plantations in the karst ecosystem of Southwestern China. Forests 9:56. https://doi.org/10.3390/f9020056
R Development Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org
Reich PB (2005) Global biogeography of plant chemistry: filling in the blanks. New Phytol 168:263–266. https://doi.org/10.1111/j.1469-8137.2005.01562.x
Reich PB, Oleksyn J (2004) Global patterns of plant leaf N and P in relation to temperature and latitude. Procs Natl Acad Sci USA 101:11001–11006. https://doi.org/10.1073/pnas.0403588101
Reich PB, Wright IJ, Lusk CH (2007) Predicting leaf physiology from simple plant and climate attributes: a global GLOPNET analysis. Ecol Appl 17:1982–1988. https://doi.org/10.1890/06-1803.1
Sardans J, Janssens IA, Alonso R, Veresoglou SD, Rillig G, Peñuelas J (2015) Foliar elemental composition of European forest tree species associated with evolutionary traits and present environmental and competitive conditions. Glob Ecol Biogeogr 24:240–255. https://doi.org/10.1111/geb.12253
Sardans J, Penuelas J (2014) Climate and taxonomy underlie different elemental concentrations and stoichiometrics of forest species: the optimum “biogeochemocal niche.” Plant Ecol 215:441–455. https://doi.org/10.1007/s11258-014-0314-2
Slik JWF, Franklin J, Arroyo-Rodriguez V et al (2018) Phylogenetic classification of the world’s tropical forests. Proc Natl Acad Sci USA 115(8):1837–1842. https://doi.org/10.1073/pnas.1714977115
Stein RJ, Höreth S, de Melo JRF, Syllwasschy L, Lee G, Garbin M (2017) Relationships between soil and leaf mineral composition are element-specific, environmental-dependent and geographically structured in the emerging model Arabidopsis halleri. New Phytol 213:1274–1286. https://doi.org/10.1111/nph.14219
Sun J, Liu B, You Y, Li W, Liu M, Shang H, He J (2019) Solar radiation regulates the leaf nitrogen and phosphorus stoichiometry across alpine meadows of the Tibetan Plateau. Agr Forest Meteorol 271:92–101. https://doi.org/10.1016/j.agrformet.2019.02.041
Sun J, Ma B, Lu X (2018) Grazing enhances soil nutrient effects: trade-offs between aboveground and belowground biomass in alpine grasslands of the Tibetan Plateau. Land Degrad Dev 29:337–348. https://doi.org/10.1002/ldr.2822
Takashima T, Hikosake K, Hirose T (2004) Photosynthesis or persistence: nitrogen allocation in leaves of evergreen and deciduous Quercus species. Plant Cell Environ 27:1047–1054. https://doi.org/10.1111/j.1365-3040.2004.01209.x
Thunjai T, Boyd CE, Dube K (2001) Poind Soil pH Measurement. J World Aquacult Soc 32:141–152. https://doi.org/10.1111/j.1749-7345.2001.tb01089.x
Townsend AR, Cleveland CC, Houlton BZ, Alden CB, White JWC (2011) Multi-element regulation of the tropical forest carbon cycle. Front Ecol Environ 9:9–17. https://doi.org/10.1890/100047
Venterink HO, Güsewell S (2010) Competitive interactions between two meadow grasses under nitrogen and phosphorus limitation. Funct Ecol 24:877–886. https://doi.org/10.1111/j.1365-2435.2010.01692.x
Wang L, Zhao G, Li M, Zhang M, Zhang L, Zhang X, An L, Xu S (2015) C:N: P stoichiometry and leaf traits of Halophytes in an arid saline environment, Northwest China. PLoS ONE 10:e0119935. https://doi.org/10.1371/journal.pone.0119935
Wei X, Deng X, Xiang W, Lei P, Ouyang S, Wen H, Chen L (2018) Calcium content and high calcium adaptation of plants in karst areas of southwestern Hunan, China. Biogeosciences 15:299–3002. https://doi.org/10.5194/bg-15-2991-2018
Wright IJ, Reich PB, Cornelissen JHC et al (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
Wu T, Wang G, Wu Q et al (2014) Patterns of leaf nitrogen and phosphorus stoichiometry among Quercus acutissima provenances across China. Ecol Complex 17:32–39. https://doi.org/10.1016/j.ecocom.2013.07.003
Wu TG, Yu MK, Wang GG, Dong Y, Cheng XR (2012) Leaf nitrogen and phosphorus stoichiometry across forty-two woody species in Southeast China. Biochem Syst Ecol 44:255–263. https://doi.org/10.1016/j.bse.2012.06.002
Zhang S, Zhang J, Slik JWF, Cao K (2012) Leaf element concentrations of terrestrial plants across China are influenced by taxonomy and the environment. Glob Ecol Biogeogr 21:809–818. https://doi.org/10.1111/j.1466-8238.2011.00729.x
Zhang L, Wang L, He W, Zhang X, An L, Xu S (2018) Patterns of leaf N: P stoichiometry along climatic gradients in sandy region, north of China. J Plant Ecol 11:218–225. https://doi.org/10.1093/jpe/rtw134
Zheng S, Shangguan Z (2007) Spatial patterns of leaf nutrient traits of the plants in the Loess Plateau of China. Trees 21:357–370. https://doi.org/10.1007/s00468-007-0129-z
Zheng W, Bao W, Gu B, He X, Leng L (2007) Carbon concentration and its characteristics in terrestrial high plants. Chin J Ecol 26:307–313 (in Chinese)
Acknowledgements
This study was financially supported by National Nature Science Foundation of China (41630752, 31670410), and the Young People Fund of Guangxi Science and Technology Department (2019GXNSFBA245036, 2019GXNSFBA245097). Special thanks to Peter Hahn for providing language help in the revision of this manuscript.
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YL and WH designed the experiment. YL, WH and TC performed the experiment and collected the leaf and soil samples. YL, LO and GN analyzed the data. YL, PZ and LZ wrote the manuscript, YL, JW, PZ and DH revised the manuscript, JW particularly modified the revised MS both in contents and English writing. All authors contributed critically to the drafts and gave final approval for publication.
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Li, Y., He, W., Wu, J. et al. Leaf stoichiometry is synergistically-driven by climate, site, soil characteristics and phylogeny in karst areas, Southwest China. Biogeochemistry 155, 283–301 (2021). https://doi.org/10.1007/s10533-021-00826-3
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DOI: https://doi.org/10.1007/s10533-021-00826-3