Advertisement

Plant and Soil

, Volume 434, Issue 1–2, pp 305–326 | Cite as

Leaf nutrient concentrations associated with phylogeny, leaf habit and soil chemistry in tropical karst seasonal rainforest tree species

  • Kundong BaiEmail author
  • Shihong Lv
  • Shijiang Ning
  • Danjuan Zeng
  • Yili Guo
  • Bin Wang
Regular Article
  • 246 Downloads

Abstract

Background and aims

Leaf nutrient concentrations are predictors of plant growth variation and crucial for biogeochemical cycling. We aimed to explore the effects of phylogeny, leaf habit and soil chemistry on leaf nutrient concentrations in tropical karst environments.

Methods

We sampled top-soils and leaves of co-existing evergreen and deciduous tree species along the continuum of mountain valley, slope and peak in a tropical karst seasonal rainforest. We used phylogenetic comparative methods to determine how leaf nutrient concentrations varied in response to phylogeny, leaf habit and soil chemistry and interacted with each other.

Results

Tree species had large inter- and intra-nutrient variability and were characterized by the combination of P limitation and Ca hyperaccumulation in leaves. The phylogenetic signals in leaf nutrient concentrations were not significant but increased with decreasing evolutionary rates as a result of the best fitted evolutionary process, i.e., stabilizing selection towards an optimum value. Compared with deciduous species, evergreen species had lower nutrient concentration requirements to fulfill specific biochemical functions in leaves. Along the valley-slope-peak continuum, the correlations between leaf and soil nutrient concentrations were positive for Ca, Mg, P, Cu and Zn and negative for N, S, K and Fe. The strength of interactions differed among leaf nutrients and this largely depended on the divergent biochemical functions among leaf nutrients.

Conclusions

Our results suggest that stabilizing selection combined with the biochemical constraints could select the locally adapted evergreen and deciduous species with sufficient phylogenetic variations to produce leaf nutrient concentrations and certain nutrient combinations that should be well-fitted in tropical karst environments.

Keywords

Tropical karst seasonal rainforest Leaf nutrient concentrations Leaf habit Soil chemistry Phylogenetic comparative methods Stabilizing selection 

Notes

Acknowledgements

We are grateful to Fujing Pan, Qingbai Lu and Dongxing Li for their assistance in conducting the field work of leaf and soil samplings. We acknowledge Xiankun Li, Wusheng Xiang and other contributors for the establishment of the permanent 15-ha Nonggang tropical karst seasonal rainforest dynamics plot. We thank anonymous reviewers for their insightful comments on the original version of the manuscript. This research was made through grants from the National Natural Science Foundation (31100285; 31360151), Guangxi Natural Science Foundation (2013GXNSFBA019079) and Guangxi Scientific and Technological Project (1355007-3) in China.

Supplementary material

11104_2018_3858_MOESM1_ESM.doc (82 kb)
Table S1 (DOC 81 kb)
11104_2018_3858_MOESM2_ESM.doc (31 kb)
Table S2 (DOC 31 kb)
11104_2018_3858_MOESM3_ESM.doc (62 kb)
Table S3 (DOC 61 kb)

References

  1. Ackerly D (2009) Conservatism and diversification of plant functional traits: evolutionary rates versus phylogenetic signal. Proc Natl Acad Sci 106:19699–19706Google Scholar
  2. Aerts R, Berendse F (1988) The effect of increased nutrient availability on vegetation dynamics in wet heathlands. Vegetatio 76:63–69Google Scholar
  3. Aerts R, Chapin FSIII (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 Google Scholar
  4. Ågren GI (2008) Stoichiometry and nutrition of plant growth in natural communities. Annu Rev Ecol Evol Syst 39:153–170.  https://doi.org/10.1146/annurev.ecolsys.39.110707.173515 Google Scholar
  5. Ågren GI, Weih M (2012) Plant stoichiometry at different scales: element concentration patterns reflect environment more than genotype. New Phytol 194:944–952.  https://doi.org/10.1111/j.1469-8137.2012.04114.x Google Scholar
  6. Álvarez-Yépiz JC, Búrquez A, Martĺnez-Yrĺzar A, Teece M, Yépez EA, Dovciak M (2017) Resource partitioning by evergreen and deciduous species in a tropical dry forest. Oecologia 183:607–618. https://doi.org.  https://doi.org/10.1007/s00442-016-3790-3 Google Scholar
  7. Anderson-Teixeira KJ, Davies AJ, Bennett AC, Gonzalez-Akre EB, Muller-Landau HC, Wright SJ, Salim KA, Zambrano AMA, Alonso A, Baltzer JL, Basset Y, Bourg NA, Broadbent EB, Brockelman WY, Bunyavejchewin S, Burslem DFRP, Butt N, Cao M, Cardenas D, Chunyong GB, Clay K, Cordell S, Dattaraja HS, Deng X, Detto M, Du X, Duque A, Erickson DL, Ewango CNE, Fischer GA, Fletcher C, Foster RB, Giardina CP, Gilbert GS, Gunatilleke N, Gunatilleke S, Hao Z, Hargrove WW, Hart TB, BCH H, He F, Hoffman FM, Howe RW, Hubbell SP, Inman-Narahari FM, Jansen PA, Jiang M, Johnson DJ, Kanzaki M, Kassim AR, Kenfack D, Kibet S, Kinnaird MF, Korte L, Kral K, Kumar J, Larson AJ, Li Y, Li X, Liu S, Lum SKY, Lutz JA, Ma K, Maddalena DM, Makana JR, Malhi Y, Marthews T, Serudin RM, McMahonSM MSWJ, Memiaghe HR, Mi X, Mizuno T, Morecroft M, Myers JA, Novotny V, de Oliveira AA, Ong PS, Orwig DA, Ostertag R, den Onden J, Parker GG, Phillips RP, Sack L, Sainge MN, Sang W, Sri-ngernyuang K, Sukumar R, Sun IF, Sungpalee W, Suresh HS, Tan S, Thomas SC, Thomas DW, Thompson J, Turner BL, Uriarte M, Valencia R, Vallejo M, Vicentini A, Vrška T, Wang X, Wang X, Weiblen G, Wolf A, Xu H, Yap S, Zimmerman J (2015) CTFS-ForestGEO: a worldwide network monitoring forests in an era of global change. Glob Chang Biol 21:828–549.  https://doi.org/10.1111/gcb.12712
  8. Bai K, He C, Wan X, Jiang D (2015) Leaf economics of evergreen and deciduous tree species along an elevational gradient in a subtropical mountain. AoB Plants 7:plv064.  https://doi.org/10.1093/aobpla/plv064 Google Scholar
  9. Blomberg SP, Garland T, Ives AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are labile. Evolution 57:717–745.  https://doi.org/10.1554/0014-3820(2003)057 Google Scholar
  10. Bremner JM (1960) Determination of nitrogen in soil by the Kjeldahl method. J Agric Sci 55:11–33.  https://doi.org/10.1017/S0021859600021572 Google Scholar
  11. Broadley MB, Bowen HC, Cotterill HL, Hammond JP, Meacham MC, Mead A, White PJ (2003) Variation in the shoot calcium content of angiosperms. J Exp Bot 54:1431–1446.  https://doi.org/10.1093/jxb/erg143 Google Scholar
  12. Broadley MB, Bowen HC, Cotterill HL, Hammond JP, Meacham MC, Mead A, White PJ (2004) Phylogenetic variation in the shoot mineral concentration of angiosperm. J Exp Bot 55:321–336.  https://doi.org/10.1093/jxb/erh002 Google Scholar
  13. Butler MA, King AA (2004) Phylogenetic comparative analysis: a modeling approach for adaptive evolution. Am Nat 164:683–695.  https://doi.org/10.1086/426002 Google Scholar
  14. Cavender-Bares J, Keen A, Miles B (2006) Phylogenetic structure of Floridian plant communites depends on taxonomic and spatial scale. Ecology 87:S109–S122.  https://doi.org/10.1890/0012-9658(2006)87 Google Scholar
  15. Chen P (1988) An observational report for soils in the Nonggang National Nature Reserve. Guihaia supp1: 52–73 (in Chinese)Google Scholar
  16. Cornelissen JHC, Pérez-Harguindeguy N, Diaz S, Grime JP, Marzano B, Cabido M, Vendramini F, Cerabolini B (1999) Leaf structure and defense control litter decomposition rate across species and life forms in regional floras on two continents. New Phytol 143:191–200Google Scholar
  17. Cornwell WK, Cornelissen JHC, Amatangelo K, Dorrepaal E, Eviner VT, Godoy O, Hobbie SE, Hoorens B, Kurokawa H, Pérez-Harguindeguy N, Quested HM, Santiago LS, Wardle DA, Wright IJ, Aerts R, Allison SD, Bodegom PV, Brovkin V, Chatain A, Callaghan TV, Díaz S, Garnier E, Gurvich DE, Kazakou E, Klein JA, Read J, Reich PB, Soudzilovskaia NA, Vaieretti MV, Westoby M (2008) Plant species traits are the predominant control on litter decomposition rates within biomass worldwide. Ecol Lett 11:1065–1071.  https://doi.org/10.1111/j.1461-0248.2008.01219.x Google Scholar
  18. Cornwell WK, Westoby M, Falster DS, FitzJohn RG, Meara BCO, Pennell MW, McGlinn DJ, Eastman JM, Moles AT, Reich PB, Tank DC, Wright IJ, Aarssen L, Beaulieu JM, Kooyman RM, Leishman MR, Miller ET, Niinemets Ü, Olksyn J, Ordonez A, Royer DL, Smith SA, Stevens PF, Warman L, Wilf P, Zanne AE (2014) Functional distinctiveness of major plant lineages. J Ecol 102:345–356.  https://doi.org/10.1111/1365-2745.12208 Google Scholar
  19. Donovan LA, Maherali H, Caruso CM, Huber H, de Kroon H (2011) The evolution of the worldwide leaf economics spectrum. Trends Ecol Evol 26:88–95.  https://doi.org/10.1016/j.tree.2010.11.011 Google Scholar
  20. Elser JJ, Acharya K, Kyle M, Cotner J, Makino W, Markow T, Watts T, Hobbie S, Fagan W, Schade J (2003) Growth rate-stoichiometry coupling in diverse biota. Ecol Lett 6:936–943.  https://doi.org/10.1046/j.1461-0248.2003.00518.x Google Scholar
  21. Felsenstein J (1973) Maximum-likelihood estimation of evolutionary trees from continuous characters. Am J Hum Genet 25:471–492Google Scholar
  22. Fernández-Martínez M, Llusià J, Filella I, Niinemets Ü, Arneth A, Wright IJ, Lereto F, Peñuelas J (2017) Nutrient-rich plants emit a less intense blend of volatile isoprenoids. New Phytol.  https://doi.org/10.1111/nph.14889
  23. Fu PL, Jiang YJ, Wang AY, Brodribb TJ, Zhang JL, Zhu SD, Cao KF (2012) Stem hydraulic traits and leaf water-stress tolerance are co-ordinated with the leaf phenology of angiosperm trees in an Asian tropical dry karst forest. Ann Bot 110:189–199.  https://doi.org/10.1093/aob/mcs092 Google Scholar
  24. Fyllas NM, Patino S, Baker TR, Bielefeld Nardoto G, Martinelli LA, Quesada CA, Paiva R, Schwarz M, Horna V, Mercado LM, Santos A, Arroyo L, Jimenez EM, Luizão FJ, Neill DA, Silva N, Prieto A, Rudas A, Silviera M, Vieira ICG, Lopez-Gonzalez G, Malhi Y, Phillips OL, Lioyd J (2009) Basin-wide variations in foliar properties of Amazonian forest: phylogeny, soils and climate. Biogeosciences 6:2677–2708.  https://doi.org/10.5194/bg-6-2677-2009 Google Scholar
  25. Garten CT (1978) Multivariate perspectives on the ecology of plant mineral element composition. Am Nat 112:533–544Google Scholar
  26. Givnish TJ (2002) Adaptive significance of evergreen vs. deciduous leaves: solving the triple paradox. Silva Fenn 36:703–743Google Scholar
  27. Gonzalez-Voyer A, Kolm N (2011) Rates of phenotypic evolution of ecological characters and sexual traits during the Tanganyikan cichlid adaptive radiation. J Evol Biol 24:2378–2388.  https://doi.org/10.1111/j.1420-9101.2011.02365.x Google Scholar
  28. Grusak MA, Broadley MR, White PJ (2016) Plant macro- and micronutrient minerals. In: eLS. John Wiley & Sons, Ltd: Chichester.  https://doi.org/10.1002/9780470015902.a0001306.pub2
  29. Guo Y, Wang B, Mallik A, Huang F, Xiang W, Ding T, Wen S, Lu S, Li D, He Y, Li X (2017) Topographic species-habitat associations of tree species in a heterogeneous tropical karst seasonal rainforest. China J Plant Ecol 10:450–460.  https://doi.org/10.1093/jpe/rtw057 Google Scholar
  30. Hall BG (2013) Building phylogenetic trees from molecular data with MEGA. Mol Biol Evol 30:1229–1235.  https://doi.org/10.1093/molbev/mst012 Google Scholar
  31. Han WX, Fang JY, Reich PB, Woodward FI, Wang ZH (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 Google Scholar
  32. 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 Google Scholar
  33. Harmon LJ, Weir JT, Brock CD, Glor RE, Challenger W (2008) GEIGER: investigating evolutionary radiations. Bioinformatics 24:129–131.  https://doi.org/10.1093/bioinformatics/btm538 Google Scholar
  34. He M, Dijkstra FA, Zhang K, Tan H, Zhao Y, Li X (2016) Influence of life form, taxonomy, climate, and soil properties on shoot and root concentration of 11 elements in herbaceous plants in a temperate desert. Plant Soil 398:339–350.  https://doi.org/10.1007/s11104-015-2669-0 Google Scholar
  35. Hernández C, Rodríguez-Serrano E, Avaria-Llautureo J, Inostroza-Michael O, Morales-Pallero B, Boric-Bargetto D, Canalles-Aguirre CB, Marquet PA, Meade A (2013) Using phylogenetic information and the comparative method to evaluate hypotheses in macroecology. Methods Ecol Evol 4:401–415.  https://doi.org/10.1111/2041-210X.12033 Google Scholar
  36. Jager MM, Richnardson SJ, Bellingham PJ, Clearwater MJ, Laughlin DC (2015) Soil fertility induces coordinated responses of multiple independent functional traits. J Ecol 103:374–385.  https://doi.org/10.1111/1365-2745.12366 Google Scholar
  37. Kamilar JM, Cooper N (2013) Phylogenetic signal in primate behavior, ecology and life history. Philos T R Soc B: Biol Sci 368:20120341.  https://doi.org/10.1098/rstb.2012.0341 Google Scholar
  38. Kerkhoff AJ, Enquist BJ (2009) Multiplicative by nature: why logarithmic transformation is necessary in allometry. J Theor Biol 257:519–521Google Scholar
  39. Kerkhoff AJ, Fagan WF, Elser JJ, Enquist BJ (2006) Phylogenetic and growth form variation in the scaling of nitrogen and phosphorus in the seed plants. Am Nat 168:E103–E122.  https://doi.org/10.1086/507879 Google Scholar
  40. Kirkby E (2012) Introduction, definition and classification of nutrients. In: Marschner P (ed) Marschner's mineral nutrition of higher plants,3rd edn. Academic Press, London, pp3–5Google Scholar
  41. Lambers H, Brundrett MC, Raven JA, Hopper SD (2010) Plant mineral nutrition in ancient landscapes: high plant species diversity on infertile soils is linked to functional diversity for nutritional strategies. Plant Soil 334:11–31.  https://doi.org/10.1007/s11104-010-0444-9 Google Scholar
  42. Lande R (1976) Natural selection and random genetic drift in phenotypic evolution. Evolution 30:314–334.  https://doi.org/10.1111/j.1558-5646.1976.tb00911.x Google Scholar
  43. Leal MC, Seehausen O, Matthews B (2017) The ecology and evolution of stoichiometric phenotypes. Trends Ecol Evol 32:108–117.  https://doi.org/10.1016/j.tree.2016.11.006 Google Scholar
  44. 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 113:873–885.  https://doi.org/10.1093/aob/mcu005 Google Scholar
  45. Losos JB (2008) Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. Ecol Lett 11:995–1007.  https://doi.org/10.1111/j.1461-0248.2008.01229.x Google Scholar
  46. Markert B (1987) The pattern of distribution of lanthanide elements in soils and plants. Phytochemistry 26:3167–3170.  https://doi.org/10.1016/S0031-9422(00)82463-2 Google Scholar
  47. Marschner P, Rengel Z (2012) Nutrient availability in soils. In: Marschner P (ed) Marschner's mineral nutrition of higher plants,3rd edn. Academic Press, London, pp315–330Google Scholar
  48. McBride MB, Richards BK, Steenhuis T, Russo JJ, Sauvé S (1997) Mobility and solubility of toxic metals and nutrients in soil fifteen years after sludge application. Soil Sci 162:487–500Google Scholar
  49. Medina E, Cuevas E, Marcano-Vega H, Meléndez-Ackerman E, Helmer EH (2017) Biogeochemical relationships of a subtropical dry forest on karst. Carib Nat 41:1–24Google Scholar
  50. Metali F, Salim KA, Burslem DFRP (2012) Evidence of foliar aluminium accumulation in local, regional and global datasets of wild plants. New Phytol 193:637–649.  https://doi.org/10.1111/j.1469-8137.2011.03965.x Google Scholar
  51. Metali F, Salim KA, Tennakoon K, Burslem DFRP (2015) Controls on foliar nutrient and aluminum concentrations in a tropical tree flora: phylogeny, soil chemistry and interactions among elements. New Phytol 205:280–292.  https://doi.org/10.1111/nph.12987 Google Scholar
  52. Monk CD (1966) An ecological significance of evergreenness. Ecology 47:504–505.  https://doi.org/10.2307/1932995 Google Scholar
  53. Neugebauer K, Broadley MR, El-Serehy HA, George TS, McNicol JW, Moraes MF, White PJ (2018) Variation in the angiosperm ionome. Physiol Plant.  https://doi.org/10.1111/ppl.12700
  54. Ordoñez JC, van Bodegom PM, Witte JM, 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 Google Scholar
  55. Orme CDL, Freckleton RP, Thomas GH, Petzoldt T, Fritz SA, Issac JB, Pearse W (2012) Caper: comparative analyses of phylogenetics and evolution in R. Methods Ecol Evol 3:145–151Google Scholar
  56. Pagel M (1994) Detecting corrected evolution on phylogenies: a general method for the comparative analysis of discrete characters. P Roy Soc B: Bio Sci 255:37–45.  https://doi.org/10.1098/rspb.1994.0006 Google Scholar
  57. Pagel M (1999) Inferring the historical patterns of biological evolution. Nature 401:877–884.  https://doi.org/10.1038/44766 Google Scholar
  58. Peñuelas J, Sardans J, Ogaya R, Estiarte M (2008) Nutrient stoichiometric relations and biogeochemical niche in coexisting plant species: effects of simulated climate change. Pol J Ecol 56:613–622Google Scholar
  59. Peñuelas J, Sardans J, Llusià J, Owen SM, Carnicer J, Giambelluca TW, Rezende EL, Waite M, Niinemets Ü (2010) Faster returns on ‘leaf economics’ and different biogeochemical niche in invasive compared with native plant species. Glob Chang Biol 16:2171–2185.  https://doi.org/10.1111/j.1365-2486.2009.02054.x Google Scholar
  60. Pornon A, Marty C, Winterton P, Lamaze T (2011) The intriguing paradox of leaf lifespan responses to nitrogen availability. Funct Ecol 25:796–801.  https://doi.org/10.1111/j.1365-2435.2011.01849.x Google Scholar
  61. R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria http://www.R-project.org Google Scholar
  62. Reich PB, Oleksyn J (2004) Global patterns of plant leaf N and P in relation to temperture and latitude. P Natl Acad Sci USA 101:11001–11006.  https://doi.org/10.1073/pnas.0403588101 Google Scholar
  63. Revell LJ, Harmon LJ, Collar DC (2008) Phylogenetic signal, evolutionary process, and rate. Syst Biol 57:591–601.  https://doi.org/10.1080/10635150802302427 Google Scholar
  64. Römheld V (2012) Diagnosis of deficiency and toxicity of nutrients. In: Marschner P (ed) Marschner's mineral nutrition of higher plants,3rd edn. Academic Press, London, pp299–311Google Scholar
  65. Sardans J, Peñuelas J (2014) Climate and taxonomy underlie different elemental concentrations and stoichiometries of forest species: the optimum “biogeochemical niche”. Plant Ecol 215:441–455.  https://doi.org/10.1007/s11258-014-0314-2 Google Scholar
  66. Sardans J, Peñuelas J (2015) Potassium: a neglected nutrient in global change. Glob Ecol Biogeogr 24:261–275.  https://doi.org/10.1111/geb.12259 Google Scholar
  67. 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 Google Scholar
  68. Sardans J, Alonso R, Carnicer J, Fernández-Martínez M (2016) Factors influencing the foliar elemental composition and stoichiometry in forest trees in Spain. Persp Plant Ecol Evol Syst 18:52–69.  https://doi.org/10.1016/j.ppees.2016.01.001 Google Scholar
  69. Su ZM, Li XK (2003) The types of natural vegetation in karst region of Guangxi and its classified system. Guihaia 23: 289–293(in Chinese)Google Scholar
  70. Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies using the neighbor-joining method. Proc Natl Acad Sci 101:11030–11035.  https://doi.org/10.1073/pnas.0404206101 Google Scholar
  71. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729.  https://doi.org/10.1093/molbev/mst197 Google Scholar
  72. Thompson K, Parkinson JA, Band SR, Spencer R (1997) A comparative study of leaf nutrient concentrations in a regional herbaceous flora. New Phytol 136:679–689.  https://doi.org/10.1046/j.1469-8137.1997.00787.x Google Scholar
  73. Townsend AR, Cleveland CC, Houlton BZ, Alden CB, White JWC (2010) Multi-element regulation of the tropical forest carbon cycle. Front Ecol Enrion 9:9–17.  https://doi.org/10.1890/100047 Google Scholar
  74. Tung Ho LS, Ané C (2014) A linear-time algorithm for Gaussian and non-Gaussian trait evolution models. Syst Biol 63:397–408.  https://doi.org/10.1093/sysbio/syu005 Google Scholar
  75. Verboom GA, Stock WD, Cramer MD (2017) Specialization to extremely low-nutrient soils limits the nutrittional adapability of plant lineages. Am Nat 189:684–699.  https://doi.org/10.1086/691449 Google Scholar
  76. Viani RAG, Rodrigues RR, Dawson TE, Lambers H, Oliveira RS (2014) Soil pH accounts for differences in species distribution and leaf nutrient concentrations of Brazilian woodland savannah and seasonally dry forest species. Perspect Plant Ecol Evol Syst 16:64–74.  https://doi.org/10.1016/j.ppees.2014.02.001 Google Scholar
  77. Wang B, Huang Y, Li X, Xiang W, Ding T, Huang F, Lu S, Han W, Wen S, He L (2014) Species composition and spatial distribution of a 15 ha northern tropical karst seasonal rainforest dynamics study plot in Nonggang, Guangxi, southern China. Biodivers Sci 22:141–156 (in Chinese).  https://doi.org/10.3724/SP.J.1003.2014.13195 Google Scholar
  78. Watanabe T, Broadley MR, Jansen S, White PJ, Takada J, Satake K, Takamatsu T, Tuah SJ, Osaki M (2007) Evolutionary control of leaf element composition in plants. New Phytol 174:516–523.  https://doi.org/10.1111/J.1469-8137.2007.02078.x Google Scholar
  79. White PJ (2012) Ion uptake mechanisms of individual cells and roots: short-distance transport. In: Marschner P (ed) Marschner's mineral nutrition of higher plants,3rd edn. Academic Press, London, pp7–47Google Scholar
  80. White PJ, Broadley MR (2003) Calcium in plants. Ann Bot 92:487–511.  https://doi.org/10.1093/aob/mcg164 Google Scholar
  81. White PJ, Brown PH (2010) Plant nutrition for sustainable development and global health. Ann Bot 105:1073–1080.  https://doi.org/10.1093/aob/mcq085 Google Scholar
  82. White PJ, Broadley MR, Thompson JA, McNicol JW, Crawley MJ, Poulton PR, Jonston AE (2012) Testing the distinctness of shoot ionomes of angiosperm families using the Rothamsted Park grass continuous Hay experiment. New Phytol 196:101–109.  https://doi.org/10.1111/j.1469-8137.2012.04228.x Google Scholar
  83. White PJ, Bowen HC, Farley E, Shaw EK, Thompson JA, Wright G, Broadley MR (2015) Phylogenetic effects on shoot magnesium concentration. Crop Pasture Sci 66:1241–1248.  https://doi.org/10.1071/CP14228 Google Scholar
  84. White PJ, Bowen HC, Broadley MR, El-Serehy HA, Neugebauer K, Taylor A, Thompson JA, Wright G (2017) Evolutionary origins of abnormally large shoot sodium accumulation in nonsaline environments within the Caryophyllales. New Phytol 214:284–293.  https://doi.org/10.1111/nph.14370 Google Scholar
  85. White PJ, Broadley MR, El-Serehy HA, George TS, Neugebauer K (2018) Linear relationships between shoot magnesium and calcium concentrations among angiosperm species are associated with cell wall chemistry. Ann Bot.  https://doi.org/10.1093/aob/mcy062
  86. Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, 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 Ü, 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 Google Scholar
  87. Yang X, Huang Z, Zhang K, Cornelissen JHC (2017) Taxonomic effect on plant base concentration and stoichiometry at the tips of the phylogeny prevails over environmental effect along a large scale gradient. Okios 126:1241–1249.  https://doi.org/10.1111/oik.04129 Google Scholar
  88. Zarcinas BA, Cartwright B, Spouncer LR (1987) Nitric acid and multi-element analysis of plant material by inductively coupled plasma spectrometry. Commun Soil Sci Plant Anal 18:131–146.  https://doi.org/10.1080/00103628709367806 Google Scholar
  89. Zhang SB, Zhang JL, Slik WF, Cao KF (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 Google Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Guangxi Key Laboratory of Plant Conservation and Restoration Ecology in Karst Terrain, Guangxi Institute of BotanyChinese Academy of SciencesGuilinChina

Personalised recommendations