Abstract
Global warming affects plant growth and leaf nutrient concentrations in temperate forests. However, the effects of warming on plants in tropical forests are poorly understood. We investigated the effects of experimental warming on the growth of four native tree species and one shrub in the model tropical forest ecosystems and evaluated leaf concentrations of carbon (C), nitrogen (N), phosphorus (P), potassium (K), calcium (Ca), and magnesium (Mg) from 2013 to 2017. We increased the temperature by translocating model forest ecosystems along two altitudinal gradients. Our results showed that, in the model tropical forests, warming increased the vertical and radial growth of Schima superba, Syzygium rehderianum, Myrsine seguinii (shrub), and Itea chinensis. However, it did not affect the vertical growth of Machilus breviflora. The radial growth of Machilus breviflora was even significantly decreased by translocation from 600 m altitude to 300 and 30 m at the end of the experiment. Warming decreased leaf N concentrations in all plant species. However, there was no consistent pattern for the effects of warming on P, K, Ca, and Mg concentrations in the leaves of all plant species. Therefore, we conclude that warming can change leaf nutrient concentrations and plant growth in tropical forests, but the responses are species-specific. Plant growth might slow down due to reduced N concentrations in the future.
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References
Allen CD, Macalady AK, Chenchouchi H, Bachelet D et al (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For Ecol Manag 259:660–684. https://doi.org/10.1016/j.foreco.2009.09.001
An YA, Wan SQ, Zhou XH, Subedar AA et al (2005) Plant nitrogen concentration, use efficiency, and contents in a tallgrass prairie ecosystem under experimental warming. Glob Chang Biol 11:1733–1744. https://doi.org/10.1111/j.1365-2486.2005.01030.x
Babita M, Maheswari M, Rao LM, Shanker AK et al (2010) Osmotic adjustment, drought tolerance and yield in castor (Ricinus communis L.) hybrids. Environ Exp Bot 69:243–249
Bremner J, Mulvaney C (1982) Nitrogen-total methods of soil analysis, part 2, chemical and microbiological properties, 2nd edn. American Society of Agronomy, Madison
Butler SM, Melillo JM, Johnson JE, Mohan J et al (2012) Soil warming alters nitrogen cycling in a New England forest: implications for ecosystem function and structure. Oecologia 168:819–828. https://doi.org/10.1007/s00442-011-2133-7
Cavaleri MA, Reed SC, Smith WK, Wood TE (2015) Urgent need for warming experiments in tropical forests. Glob Chang Biol 21:2111–2121. https://doi.org/10.1111/gcb.12860
Cakmak I (2005) The role of potassium in alleviating detrimental effects of abiotic stresses in plants. J Plant Nutr Soil Sci 168:521–530. https://doi.org/10.1002/jpln.200420485
Chapin FS, Matson PA, Vitousek PK (2011) Principles of terrestrial ecosystems ecology. Springer, New York
Cregger MA, McDowell NG, Pangle RE, Pockman WT et al (2014) The impact of precipitation change on nitrogen cycling in a semiarid ecosystem. Funct Ecol 28:1534–1544. https://doi.org/10.1111/1365-2435.12282
Cunningham S, Read J (2002) Comparison of temperate and tropical rainforest tree species: photosynthetic responses to growth temperature. Oecologia 133:112–119. https://doi.org/10.1007/s00442-002-1034-1
Devi N, Hagedorn F, Moiseev P, Bugmann H et al (2008) Expanding forests and changing growth forms of Siberian larch at the Polar Urals treeline during the 20th century. Glob Chang Biol 18:448–456. https://doi.org/10.1111/j.1365-2486.2008.01583.x
D’Orangeville L, Houle D, Côté B, Duchesne L (2014) Soil response to a 3-year increase in temperature and nitrogen deposition measured in a mature boreal forest using ion-exchange membranes. Environ Monit Assess 186:8191–8202. https://doi.org/10.1007/s10661-014-3997-x
Drake JE, Tjoelker MG, Aspinwall MJ, Reich PB et al (2018) The partitioning of gross primary production for young Eucalyptus tereticornis trees under experimental warming and altered water availability. New Phytol 222:1298–1312. https://doi.org/10.1111/nph.15629
Fang X, Zhou GY, Li YL, Liu SZ et al (2016) Warming effects on biomass and composition of microbial communities and enzyme activities within soil aggregates in subtropical forest. Biol Fert Soils 52:353–365. https://doi.org/10.1007/s00374-015-1081-5
Gargallo-Garriga A, Sardans J, Pérez-Trujillo M, Oravec M et al (2015) Warming differentially influences the effects of drought on stoichiometry and metabolomics in shoots and roots. New Phytol 207:591–603. https://doi.org/10.1111/nph.13377
Gerdol R, Marchesini R, Iacumin P (2017) Bedrock geology interacts with altitude in affecting leaf growth and foliar nutrient status of mountain vascular plants. J Plant Ecol 10:839–850. https://doi.org/10.1093/jpe/rtw092
Gonzalez-Meler MA, Silva LBC, Dias-De-Oliveira E, Flower CE et al (2017) Experimental air warming of a Stylosanthes capitata, Vogel dominated tropical pasture affects soil respiration and nitrogen dynamics. Front. Plant Sci. https://doi.org/10.3389/fpls.2017.00046
Giordano CV, Guevara A, Boccalandro HE, Stator C et al (2011) Water status, drought responses, and growth of Prosopis flexuosa trees with different access to the water table in a warm South American desert. Plant Ecol 212:1123–1134. https://doi.org/10.1007/s11258-010-9892-9
Graça MAS, Poquet JM (2014) Do climate and soil influence phenotypic variability in leaf litter, microbial decomposition and shredder consumption? Oecologia 174:1021–1032. https://doi.org/10.1007/s00442-013-2825-2
Han W, Fang J, Guo D, Zhang Y (2005) Leaf nitrogen and phosphorus stoichiometry across 753 terrestrial plant species in China. New Phytol 168:377–385. https://doi.org/10.1111/j.1469-8137.2005.01530.x
Hochmal AK, Schulze S, Trompelt K, Hippler M (2015) Calcium-dependent regulation of photosynthesis. Biochim Biophys Acta 1847:993–1003. https://doi.org/10.1016/j.bbabio.2015.02.010
Hoeber S, Leuschner C, Kohler L, Arias-Aguilar D et al (2014) The importance of hydraulic conductivity and wood density to growth performance in eight tree species from a tropical semi-dry climate. For Ecol Manag 330:126–136. https://doi.org/10.1016/j.foreco.2014.06.039
IPCC (2018) An Intergovernmental Panel on Climate Change special report on the impacts of global warming of 1.5 °C. IPCC, Geneva
Kang HZ, Zhuang HL, Wu LL, Liu QL et al (2011) Variation in leaf nitrogen and phosphorus stoichiometry in Picea abies across Europe: an analysis based on local observations. For Ecol Manag 261:195–202. https://doi.org/10.1016/j.foreco.2010.10.004
Leon-Sanchez L, Nicolas E, Nortes PA, Maestre FT et al (2016) Photosynthesis and growth reduction with warming are driven by nonstomatal limitations in a Mediterranean semi-arid shrub. Ecol Evol 6:2725–2738. https://doi.org/10.1002/ece3.2074
Li Y, Niu SL, Yu GR (2016a) Aggravated phosphorus limitation on biomass production under increasing nitrogen loading: a meta-analysis. Funct Ecol 22:934–943. https://doi.org/10.1111/gcb.13125
Li YY, Liu JX, Zhou GY, Huang WJ et al (2016b) Warming effects on photosynthesis of subtropical tree species: a translocation experiment along an altitudinal gradient. Sci Rep 6:24895. https://doi.org/10.1038/srep24895
Li YY, Zhou GY, Liu JX (2017) Different growth and physiological response of six subtropical tree species to warming. Front Plant Sci. https://doi.org/10.3389/fpls.2017.01511
Liu B, Liang E, Liu K, Camarero JJ (2018) Species- and elevation-dependent growth responses to climate warming of Mountain forests in the Qinling Mountain. Certral China. Forest 9:5. https://doi.org/10.3390/f9050248
Liu HY, Williams AP, Allen CD, Guo DL et al (2013) Rapid warming accelerates tree growth decline in semi-arid forests of Inner Asia. Glob Chang Biol 19:2500–2510. https://doi.org/10.1111/gcb.12217
Liu JX, Liu SG, Li YY, Liu SZ et al (2017a) Warming effects on the decomposition of two litter species in model subtropical forests. Plant Soil 420:277–287. https://doi.org/10.1007/s11104-017-3392-9
Liu YC, Liu SR, Wan SQ, Wang JX et al (2017b) Effects of experimental throughfall reduction and soil warming on fine root biomass and its decomposition in a warm temperate oak forest. Soi total environ 574:1448–1455. https://doi.org/10.1016/j.scitotenv.2016.08.116
Lloyd J, Farquhar GD (2008) Effects of rising temperatures and [CO2] on the physiology of tropical forest trees. Philosophical Transactions of the Royal Society of London B: Biological Sciences 363:1811–1817. https://doi.org/10.1098/rstb.2007.0032
Mantgem PJ, Stephenson NL, Byrne JC, Daniels LD et al (2009) Widespread increase of tree mortality rates in the western United States. Science 323:521–524. https://doi.org/10.1126/science.1165000
Mengutay M, Ceylan Y, Kutman UB, Cakmak I (2013) Adequate magnesium nutrition mitigates adverse effects of heat stress on maize and wheat. Plant Soil 368:57–72. https://doi.org/10.1007/s11104-013-1761-6
Nelson DW, Sommers LE (1982) Carbon and organic matter. In: Page AL, Mille RH, Keeney DR (eds) Methods of soil analysis—part 2: chemical and microbiological properties. American Society of Agronomy, Madison, pp 561–579
Reich PB, Oleksyn J (2004) Global patterns of plant leaf N and P in relation to temperature and latitude. Proc Natl Acad Sci USA 101:11001–11006. https://doi.org/10.1073/pnas.0403588101
Reich PB, Oleksyn J, Wright IJ (2009) Leaf phosphorus influences the photosynthesis–nitrogen relation: a cross-biome analysis of 314 species. Oecologia 160:207–212. https://doi.org/10.1007/s00442-009-1291-3
Reich PB, Walters MB, Tjoelker MG, Vanderklein D, Buschena C (1998) Photosynthesis and respiration rates depend on leaf and root morphology and nitrogen concentration in nine boreal tree species differing in relative growth rate. Funct Ecol 12:395–405. https://doi.org/10.1046/j.1365-2435.1998.00209.x
Rivas-Ubach A, Sardans J, Perez-Trujillo M, Estiarte M et al (2012) Strong relationship between elemental stoichiometry and metabolome in plants. Proc Natl Acad Sci USA 109:4181–4186. https://doi.org/10.1073/pnas.1116092109
Rodgers VL, Smith NG, Hoeppner SS, Dukes JS (2018) Warming increases the sensitivity of seeding growth capacity to rainfall in six temperate deciduous tree species. Aob Plants. https://doi.org/10.1093/aobpla/ply003
Sager EPS, Hutchinson TC (2006) Responses of secondary chemicals in sugar maple (Acer saccharum) seedlings to UV-B, springtime warming and nitrogen additions. Tree Physiol 26:1351–1361. https://doi.org/10.1093/treephys/26.10.1351
Sardans J, Peñuelas J (2005) Drought decreases soil enzyme activity in a Mediterranean Quercus ilex L. forest. Soil Biol Biochem 37:455–461. https://doi.org/10.1016/j.soilbio.2004.08.004
Sardans J, Peñuelas J, Prieto P, Estiarte M (2008) Changes in Ca, Fe, Mg, Mo, Na, and S content in a Mediterranean shrubland under warming and drought. J Geophys Res. https://doi.org/10.1029/2008jg000795
Sardans J, Peñuelas J, Coll M, Vayreda J et al (2012) Stoichiometry of potassium is largely determined by water availability and growth in Catalonian forests. Funct Ecol 26:1077–1089. https://doi.org/10.1111/j.1365-2435.2012.02023.x
Sardans J, Rivas-Ubach A, Estiarte M, Ogaya R et al (2013) Field-simulated droughts affect elemental leaf stoichiometry in Mediterranean forests and shrublands. Acta Oecol 50:20–31. https://doi.org/10.1016/j.actao.2013.04.002
Soto-Correa JC, Saenz-Romero C, Lindig-Cisneros R, de la Barrera R et al (2013) The neotropical shrub Lupinus elegans, from temperate forests, may not adapt to climate change. Plant Biol 15:607–610. https://doi.org/10.1111/j.1438-8677.2012.00716.x
Stinziano JR, Huner NP, Way DA (2015) Warming delays autumn declines in photosynthetic capacity in a boreal conifer, Norway spruce (Picea abies). Tree Physiol 35:1303–1313. https://doi.org/10.1093/treephys/tpv118
Sullivan PF, Ellison SBZ, McNown RW, Brownlee AH et al (2015) Evidence of soil nutrient availability as the proximate constraint on growth of treeline trees in northwest Alaska. Ecology 96:716–727. https://doi.org/10.1890/14-0626.1
Thomas DS, Montagu KD, Conroy JP (2006) Leaf inorganic phosphorus as a potential indicator of phosphorus status, photosynthesis and growth of Eucalyptus grandis seedlings. For Ecol Manag 223:267–274. https://doi.org/10.1016/j.foreco.2005.11.006
Tjoelker MG, Reich PB, Oleksyn J (1999) Changes in leaf nitrogen and carbohydrates underlie temperature and CO2 acclimation of dark respiration in five boreal tree species. Plant, Cell Environ 22:767–778. https://doi.org/10.1046/j.1365-3040.1999.00435.x
Tripler CE, Kaushal SS, Likens GE, Walter MT (2006) Patterns in potassium dynamics in forest ecosystems. Ecol Lett 9:451–466. https://doi.org/10.1111/j.1461-0248.2006.00891.x
Wan SQ, Hui DF, Wallace L, Luo YQ (2005) Direct and indirect effects of experimental warming on ecosystem carbon processes in a tallgrass prairie. Glob Biogeochem Cycles. https://doi.org/10.1029/2004gb002315
Wang WZ, Jia M, Wang GX, Zhu WZ et al (2017) Rapid warming forces contrasting growth trends of subalpine fir (Abies fabri) at higher- and lower-elevations in the eastern Tibetan Plateau. For Ecol Manag 402:135–144. https://doi.org/10.1016/j.foreco.2017.07.043
Way DA, Oren R (2010) Differential responses to changes in growth temperature between trees from different functional groups and biomes: a review and synthesis of data. Tree Physiol 30:669–688. https://doi.org/10.1093/treephys/tpq015
Wu GL, Liu H, Hua L, Luo W et al (2018) Differential responses of stomata and photosynthesis to elevated temperature in two co-occurring subtropical forest tree species. Front Plant Sci 9:467. https://doi.org/10.3389/fpls.2018.00467
Wu X, Liu H, Wang Y, Deng M (2013) Prolonged limitation of tree growth due to warmer spring in semi-arid mountain forests of Tianshan, northwest China. Environ Res Lett 8:024016. https://doi.org/10.1088/1748-9326/8/2/024016
Yuan YG, Ge LT, Yang HS, Ren WZ (2017) A meta-analysis of experimental warming effects on woody plant growth and photosynthesis in forests. J For Res 29:727–733. https://doi.org/10.1007/s11676-017-0499-z
Yue K, Fornara DA, Yang WQ, Peng Y et al (2017) Effects of three global change drivers on terrestrial C:N:P stoichiometry: a global synthesis. Glob Change Biol 23:2450–2463. https://doi.org/10.1111/gcb.13569
Zhang QF, Xie JS, Lyu MK, Xiong DC et al (2017) Short-term effects of soil warming and nitrogen addition on the N: P stoichiometry of Cunninghamia lanceolata in subtropical regions. Plant Soil 411:395–407. https://doi.org/10.1007/s11104-016-3037-4
Zhou GY, Wei XH, Wu YP, Liu SG et al (2011) Quantifying the hydrological responses to climate change in an intact forested small watershed in southern China. Glob Chang Biol 12:3736–3746. https://doi.org/10.1111/j.1365-2486.2011.02499.x
Acknowledgements
This study was jointly funded by the National Natural Science Foundation of China (Grant Nos. 31570482 and 31670487), Science and technology innovation project of Guangdong Province forestry (Grant No. 2019KJCX023), Key Research Program of Frontier Sciences, CAS (Y621231001) and the Guangdong Hundred, Thousand and Ten Thousand Talents Program.
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Wu, T., Qu, C., Li, Y. et al. Warming effects on leaf nutrients and plant growth in tropical forests. Plant Ecol 220, 663–674 (2019). https://doi.org/10.1007/s11258-019-00943-y
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DOI: https://doi.org/10.1007/s11258-019-00943-y