Warming effects on morphological and physiological performances of four subtropical montane tree species

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Key message

In a downward transplantation experiment, warming stimulated growth and photosynthesis of Schima superba Gardn. et Champ., Syzygium rehderianum Merr. et Perry and Itea chinensis Hook. et Arn. via increased stomatal conductance. Warming had no effect on growth of Machilus breviflora (Benth.) Hemsl., indicating species-specific differences in response to warming.


Climate change has been shown to shift species composition and community structure in subtropical forests. Thus, understanding the species-specific responses of growth and physiological processes to warming is essential.


To investigate how climate warming affects growth, morphological and physiological performance of co-occurring tree species when they are growing at different altitudes.


Soils and 1-year-old seedlings of four subtropical co-occurring tree species (Schima superba Gardn. et Champ., Syzygium rehderianum Merr. et Perry, Itea chinensis Hook. et Arn. and Machilus breviflora (Benth.) Hemsl.) were transplanted to three altitudes (600 m, 300 m and 30 m a.s.l.), inducing an effective warming of 1.0 °C and 1.5 °C. Growth, morphological, and physiological performances of these seedlings were monitored.


When exposed to warmer conditions, aboveground growth of the four species except M. breviflora was strongly promoted, accompanied by increased light-saturated photosynthetic rate and stomatal conductance. Warming also significantly increased concentrations of non-structural carbohydrates in leaves of S. rehderianum and M. breviflora, stems of S. superba and S. rehderianum, and roots of I. chinensis. However, we did not detect any effect of warming on stomatal length and stomatal density.


Our results provide evidence that climate warming could have species-specific impacts on co-occurring tree species, which might subsequently shift species composition and forest structure.

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  1. Anadon-Rosell A, Dawes MA, Fonti P, Hagedorn F, Rixen C, von Arx G (2018) Xylem anatomical and growth responses of the dwarf shrub Vaccinium myrtillus to experimental CO2 enrichment and soil warming at treeline. Sci Total Environ 642:1172–1183

  2. Aspinwall MJ, Drake JE, Campany C, Vårhammar A, Ghannoum O, Tissue DT, Reich PB, Tjoelker MG (2016) Convergent acclimation of leaf photosynthesis and respiration to prevailing ambient temperatures under current and warmer climates in Eucalyptus tereticornis. New Phytol 212:354–367

  3. Barbosa C, Pugnaire FI, Peroni N, Castellani TT (2018) Warming effects on the colonization of a coastal ecosystem by Furcraea foetida (Asparagaceae), a clonal invasive species. Plant Ecol 219:813–821

  4. Burke M, Hsiang SM, Miguel E (2015) Global non-linear effect of temperature on economic production. Nature 527:235–239

  5. Cheesman AW, Klaus W (2013) Elevated night-time temperatures increase growth in seedlings of two tropical pioneer tree species. New Phytol 197:1185–1192

  6. Clark DB, Clark DA, Oberbauer SF (2010) Annual wood production in a tropical rain forest in NE Costa Rica linked to climatic variation but not to increasing CO2. Glob Chang Biol 16:747–759

  7. Clark DA, Clark DB, Oberbauer SF (2014) Field-quantified response of tropical rainforest aboveground productivity to increasing CO2 and climatic stress, 1997–2009. J Geophys Res-Biogeo 118:783–794

  8. Dietze MC, Sala A, Carbone MS, Czimczik CI, Mantooth JA, Richardson AD, Vargas R (2014) Nonstructural carbon in woody plants. Annu Rev Plant Biol 65:667–687

  9. Djanaguiraman M, Prasad PVV, Boyle DL, Schapaugh WT (2011) High-temperature stress and soybean leaves: leaf anatomy and photosynthesis. Crop Sci 51:2125–2131

  10. Drake JE, Aspinwall MJ, Pfautsch S, Rymer PD, Reich PB, Smith RA, Crous KY, Tissue DT, Ghannoum O, Tjoelker MG (2015) The capacity to cope with climate warming declines from temperate to tropical latitudes in two widely distributed Eucalyptus species. Glob Chang Biol 21:459–472

  11. Duursma R, Barton C, Lin Y, Medlyn B, Eamus D, Tissue D, Ellsworth D, McMurtrie R (2014) The peaked response of transpiration rate to vapour pressure deficit in field conditions can be explained by the temperature optimum of photosynthesis. Agric For Meteorol 189:2–10

  12. Ebell L (1969) Variation in total soluble sugars of conifer tissues with method of analysis. Phytochemistry 8:227–233

  13. Fahey C, Winter K, Slot M, Kitajima K (2016) Influence of arbuscular mycorrhizal colonization on whole-plant respiration and thermal acclimation of tropical tree seedlings. Ecol Evol 6:859–870

  14. Franks PJ, Doheny-Adams TW, Britton-Harper ZJ, Gray JE (2015) Increasing water-use efficiency directly through genetic manipulation of stomatal density. New Phytol 207:188–195

  15. Gratani L (2014) Plant phenotypic plasticity in response to environmental factors. Adv Bot 2014:17

  16. Gunderson CA, O'hara KH, Campion CM, Walker AV, Edwards NT (2010) Thermal plasticity of photosynthesis: the role of acclimation in forest responses to a warming climate. Glob Chang Biol 16:2272–2286

  17. Hamann E, Kesselring H, Stöcklin J (2018) Plant responses to simulated warming and drought: a comparative study of functional plasticity between congeneric mid and high elevation species. J Plant Ecol 11:364–374

  18. Hartmann H, Trumbore S (2016) Understanding the roles of nonstructural carbohydrates in forest trees–from what we can measure to what we want to know. New Phytol 211:386–403

  19. Hepworth C, Doheny-Adams T, Hunt L, Cameron DD, Gray JE (2015) Manipulating stomatal density enhances drought tolerance without deleterious effect on nutrient uptake. New Phytol 208:336–341

  20. IPCC (2014) Summary for policymakers. In: Field CB, Barros VR, Mastrandrea MD, Mach KJ, MAK A, Adger N, Anokhin YA, Anisimov OA, Arent DJ, Barnett J, Burkett V, Cai R (eds) Climate Change 2014: Impacts, Adaptation, and Vulnerability. Part A: Global and Sectoral Aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge and NY pp 1–32

  21. Jump AS, Hunt JM, Penuelas J (2006) Rapid climate change-related growth decline at the southern range edge of Fagus sylvatica. Glob Chang Biol 12:2163–2174

  22. Kooyers NJ, Greenlee AB, Colicchio JM, Oh M, Blackman BK (2014) Replicate altitudinal clines reveal that evolutionary flexibility underlies adaptation to drought stress in annual Mimulus guttatus. New Phytol 206:152–165

  23. Kozlowski TT (1992) Carbohydrate sources and sinks in woody plants. Bot Rev 58:107–222

  24. Liu J, Liu S, Li Y, Liu S, Yin G, Huang J, Xu Y, Zhou G (2017) Warming effects on the decomposition of two litter species in model subtropical forests. Plant Soil 420:277–287

  25. Marias DE, Meinzer FC, Woodruff DR, Mcculloh KA (2016) Thermotolerance and heat stress responses of Douglas-fir and ponderosa pine seedling populations from contrasting climates. Tree Physiol 37:301–315

  26. Peñuelas J, Ogaya R, Boada M, Jump AS (2007) Migration, invasion and decline: changes in recruitment and forest structure in a warming-linked shift of European beech forest in Catalonia (NE Spain). Ecography 30:829–837

  27. Perez-Harguindeguy N, Diaz S, Garnier E, Lavorel S, Poorter H, Jaureguiberry P et al (2013) New handbook for standardised measurement of plant functional traits worldwide. Aust J Bot 61:167–234

  28. Poorter H, Niinemets Ü, Poorter L, Wright IJ, Villar R (2009) Causes and consequences of variation in leaf mass per area (LMA): a meta–analysis. New Phytol 182:565–588

  29. Prieto P, Peñuelas J, Llusià J, Asensio D, Estiarte M (2009) Effects of long-term experimental night-time warming and drought on photosynthesis, Fv/Fm and stomatal conductance in the dominant species of a Mediterranean shrubland. Acta Physiol Plant 31:729–739

  30. Rodgers VL, Smith NG, Hoeppner SS, Dukes JS (2018) Warming increases the sensitivity of seedling growth capacity to rainfall in six temperate deciduous tree species. Aob Plants 10(1):ply003.

  31. Salinas N, Malhi Y, Meir P, Silman M, Roman Cuesta R, Huaman J, Salinas D, Huaman V, Gibaja A, Mamani M, Farfan F (2011) The sensitivity of tropical leaf litter decomposition to temperature: results from a large-scale leaf translocation experiment along an elevation gradient in Peruvian forests. New Phytol 189:967–977

  32. Salvucci ME, Crafts-Brandner SJ (2004) Inhibition of photosynthesis by heat stress: the activation state of Rubisco as a limiting factor in photosynthesis. Physiol Plant 120:179–186

  33. Sheldon KS, Yang S, Tewksbury JJ (2011) Climate change and community disassembly: impacts of warming on tropical and temperate montane community structure. Ecol Lett 14:1191–1200

  34. Slot M, Winter K (2017) Photosynthetic acclimation to warming in tropical forest tree seedlings. J Exp Bot 68:2275–2284

  35. Slot M, Winter K (2018) High tolerance of tropical sapling growth and gas exchange to moderate warming. Funct Ecol 32:599–611

  36. Tang B, Yin C, Wang Y, Sun Y, Liu Q (2016) Positive effects of night warming on physiology of coniferous trees in late growing season: leaf and root. Acta Oecol-Int J Ecol 73:21–30

  37. Thomas CD, Cameron A, Green RE, Bakkenes M, Beaumont LJ, Collingham YC, Erasmus BF, de Siqueira MF, Grainger A, Hannah L, Hughes L, Huntley B, van Jaarsveld A, Midgley GF, Miles L, Ortega-Huerta MA, Peterson AT, Phillips OL, Williams SE (2004) Extinction risk from climate change. Nature 427:145–148

  38. Trahan MW, Schubert BA (2016) Temperature-induced water stress in high-latitude forests in response to natural and anthropogenic warming. Glob Chang Biol 22:782–791

  39. Walker TWN, Weckwerth W, Bragazza L, Fragner L, Forde BG, Ostle NJ, Signarbieux C, Sun X, Ward SE, Bardgett RD (2018) Plastic and genetic responses of a common sedge to warming have contrasting effects on carbon cycle processes. Ecol Lett 22:159–169

  40. Wang J, Duan B, Zhang Y (2012) Effects of experimental warming on growth, biomass allocation, and needle chemistry of Abies faxoniana in even-aged monospecific stands. Plant Ecol 213:47–55

  41. 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

  42. Way DA, Oren R, Kroner Y (2015) The space-time continuum: the effects of elevated CO2 and temperature on trees and the importance of scaling. Plant Cell Environ 38:991–1007

  43. Wertin TM, McGuire MA, Teskey RO (2011) Higher growth temperatures decreased net carbon assimilation and biomass accumulation of northern red oak seedlings near the southern limit of the species range. Tree Physiol 31:1277–1288

  44. Wu G, Liu H, Hua L, Luo Q, Lin Y, He P, Feng S, Liu J, Ye Q (2018) Differential responses of stomata and photosynthesis to elevated temperature in two co-occurring subtropical forest tree species. Front Plant Sci 9:467.

  45. Wu T, Qu C, Li Y, Li X, Zhou G, Liu S, Chu G, Meng Z, Lie Z, Liu J (2019) Warming effects on leaf nutrients and plant growth in tropical forests. Plant Ecol 220:663–674

  46. Xu C-Y, Salih A, Ghannoum O, Tissue DT (2012) Leaf structural characteristics are less important than leaf chemical properties in determining the response of leaf mass per area and photosynthesis of Eucalyptus saligna to industrial-age changes in [CO2] and temperature. J Exp Bot 63:5829–5841

  47. Xu Z, Jiang Y, Jia B, Zhou G (2016) Elevated-CO2 response of stomata and its dependence on environmental factors. Front Plant Sci 7:657.

  48. Yuan Y, Ge L, Yang H, Ren W (2018) A meta-analysis of experimental warming effects on woody plant growth and photosynthesis in forests. J For Res 29:727–733

  49. Zheng Y, Guo L, Hou R, Zhou H, Hao L, Li F, Cheng D, Peng Z, Xu M (2018) Experimental warming enhances the carbon gain but does not affect the yield of maize (Zea mays L.) in the North China plain. Flora 240:152–163

  50. Zhou G, Wei X, Wu Y, Liu S, Huang Y, Yan J, Zhang D, Zhang Q, Liu J, Meng Z, Wang C, Chu G, Liu S, Tang X, Liu X (2011) Quantifying the hydrological responses to climate change in an intact forested small watershed in southern China. Glob Chang Biol 17:3736–3746

  51. Zhou G, Peng C, Li Y, Liu S, Zhang Q, Tang X, Liu J, Yan J, Zhang D, Chu G (2013) A climate change-induced threat to the ecological resilience of a subtropical monsoon evergreen broad-leaved forest in southern China. Glob Chang Biol 19:1197–1210

  52. Zhou G, Houlton BZ, Wang W, Huang W, Xiao Y, Zhang Q, Liu S, Cao M, Wang X, Wang S (2014) Substantial reorganization of China’s tropical and subtropical forests: based on the permanent plots. Glob Chang Biol 20:240–250

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We thank the editor and the two anonymous reviewers for valuable comments.

Data availability statement

The datasets generated during and/or analyzed during the current study are not publicly available because the authors are working on another manuscript using the same dataset but are available from the corresponding author on reasonable request.

Funding information

This study was jointly funded by the National Natural Science Foundation of China (31800511, 31570482 and 31670453), the Science and Technology Innovation Project of Guangdong Province Forestry (Grant No. 2019KJCX023), and the Fund of Key Laboratory of Vegetation Restoration and Management of Degraded Ecosystems, Chinese Academy of Sciences (DE2018028).

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Correspondence to Juxiu Liu.

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We declare that this study have obtained the appropriate permissions from the responsible authorities of “Dinghushan Biosphere Reserve.”

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Contribution of co-authors JL and GZ conceived this study; YL, YX, TW, SL, and JW conducted the experiment; YL analyzed the results. All the authors contributed to writing and editing the manuscript.

Handling Editor: Marcus Schaub

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Li, Y., Xu, Y., Li, Y. et al. Warming effects on morphological and physiological performances of four subtropical montane tree species. Annals of Forest Science 77, 2 (2020).

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  • Transplantation
  • Photosynthesis
  • Growth
  • Stomatal traits
  • Non-structural carbohydrates