Effects of elevation on spring phenological sensitivity to temperature in Tibetan Plateau grasslands


Vegetation phenology is an important indicator of climate change impacts on the seasonal dynamics of the biosphere. However, little is known about the influence of elevation on spring phenological sensitivity to temperature in an alpine ecosystem. Based on remotely sensed land surface phenology and temperature data from 2001 to 2010, this study investigated the rate of spring phenological change of the Tibetan Plateau (TP) grasslands in response to interannual temperature variations at different elevations. Results suggest that spring phenology in the TP grasslands exhibits a stronger response to changes in temperature at higher elevations than at lower ones. In particular, spring phenology advanced by 1–2 days in response to a 1 °C increase in May average temperature at elevations from 3,000 to 3,500 m, while the rate was up to 8–9 days/°C at 5,000–5,500 m. Analysis using accumulated growing degree days (AGDD) from January 1 through May 31 showed the same general trend with increased elevation associated with increased sensitivity (as measured by phenological change per unit of AGDD change). Such temperature sensitivity gradients in the TP grasslands could be partly explained by the growth efficiency hypothesis which suggests that vegetation adapted to colder climates likely requires less heat energy for the onset of growing season and vice versa in warmer climates. Furthermore, accumulated growing degree days from January 1 to the greenup date were found to decrease with increasing elevations, which provided evidence to support the applicability of the growth efficiency hypothesis in an alpine grassland ecosystem.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3


  1. 1.

    Bertin RI (2008) Plant phenology and distribution in relation to recent climate change. J Torrey Bot Soc 135:126–146

    Article  Google Scholar 

  2. 2.

    Chen XQ, Hu B, Yu R (2005) Spatial and temporal variation of phenological growing season and climate change impacts in temperate eastern China. Glob Change Biol 11:1118–1130

    Article  Google Scholar 

  3. 3.

    Cleland EE, Chuine I, Menzel A et al (2007) Shifting plant phenology in response to global change. Trends Ecol Evol 22:357–365

    Article  Google Scholar 

  4. 4.

    Menzel A, Sparks T, Estrella N et al (2006) European phenological response to climate change matches the warming pattern. Glob Change Biol 12:1969–1976

    Article  Google Scholar 

  5. 5.

    Yu HY, Luedeling E, Xu JC (2010) Winter and spring warming result in delayed spring phenology on the Tibetan Plateau. Proc Natl Acad Sci USA 107:22151–22156

    Article  Google Scholar 

  6. 6.

    Fitter AH, Fitter RSR, Harris ITB et al (1995) Relationships between first flowering date and temperature in the flora of a locality in central England. Funct Ecol 91:55–60

    Article  Google Scholar 

  7. 7.

    Sparks TH, Jeffree EP, Jeffree CE (2000) An examination of the relationship between flowering times and temperature at the national scale using long-term phenological records from the UK. Int J Biometeorol 44:82–87

    Article  Google Scholar 

  8. 8.

    Donnelly A, Salamin N, Jones MB (2006) Changes in tree phenology: an indicator of spring warming in Ireland? Biol Environ P Roy Irish Acad 106:49–56

    Article  Google Scholar 

  9. 9.

    Menzel A (2003) Plant phenological anomalies in Germany and their relation to air temperature and NAO. Clim Change 57:243–263

    Article  Google Scholar 

  10. 10.

    Gordo O, Sanz JJ (2009) Long-term temporal changes of plant phenology in the Western Mediterranean. Glob Change Biol 15:1930–1948

    Article  Google Scholar 

  11. 11.

    Qiu BW, Zhong M, Tang ZH et al (2013) Spatiotemporal variability of vegetation phenology with reference to altitude and climate in the subtropical mountain and hill region, China. Chin Sci Bull 58:2883–2892

    Article  Google Scholar 

  12. 12.

    Zheng JY, Ge QS, Hao ZX (2002) Impacts of climate warming on plants phenophases in China for the last 40 years. Chin Sci Bull 47:1826–1831

    Article  Google Scholar 

  13. 13.

    Hopkins AD (1920) The bioclimatic law. J Wash Acad Sci 10:34–40

    Google Scholar 

  14. 14.

    Rötzer T, Chmielewski FM (2001) Phenological maps of Europe. Clim Res 18:249–257

    Article  Google Scholar 

  15. 15.

    Dunn AH, de Beurs KM (2011) Land surface phenology of North American mountain environments using moderate resolution imaging spectroradiometer data. Remote Sens Environ 115:1220–1233

    Article  Google Scholar 

  16. 16.

    Dittmar C, Elling W (2006) Phenological phases of common beech (Fagus sylvatica L.) and their dependence on region and altitude in Southern Germany. Eur J For Res 125:181–188

    Article  Google Scholar 

  17. 17.

    Čufar K, Luis MD, Saz MA et al (2012) Temporal shifts in leaf phenology of beech (Fagus sylvatica) depend on elevation. Trees 26:1091–1100

    Article  Google Scholar 

  18. 18.

    Vitasse Y, Delzon S, Dufrêne E et al (2009) Leaf phenology sensitivity to temperature in European trees: do within-species populations exhibit similar responses? Agr For Meteorol 149:735–744

    Article  Google Scholar 

  19. 19.

    Ziello C, Estrella N, Kostova M et al (2009) Influence of altitude on phenology of selected plant species in the Alpine region (1971–2000). Clim Res 39:227–234

    Article  Google Scholar 

  20. 20.

    Vitasse Y, Bresson CC, Kremer A et al (2010) Quantifying phenological plasticity to temperature in two temperate tree species. Funct Ecol 24:1211–1218

    Article  Google Scholar 

  21. 21.

    Körner C (2004) Mountain biodiversity, its causes and function. Ambio 13:11–17

    Google Scholar 

  22. 22.

    Yao TD, Liu XD, Wang NL et al (2000) Amplitude of climatic changes in Qinghai-Tibetan Plateau. Chin Sci Bull 45:1236–1243

    Article  Google Scholar 

  23. 23.

    Cannone N, Diolaiuti G, Guglielmin M et al (2008) Accelerating climate change impacts on alpine glacier forefield ecosystems in the European Alps. Ecol Appl 18:637–648

    Article  Google Scholar 

  24. 24.

    Dong MY, Jiang Y, Zheng CT et al (2012) Trends in the thermal growing season throughout the Tibetan Plateau during 1960–2009. Agr For Meteorol 166–167:201–206

    Article  Google Scholar 

  25. 25.

    Pigliucci M, Murren CJ, Schlichting CD (2006) Phenotypic plasticity and evolution by genetic assimilation. J Exp Biol 209:2362–2367

    Article  Google Scholar 

  26. 26.

    Kramer K, Degen B, Buschbom J et al (2010) Modelling exploration of the future of European beech (Fagus sylvatica L.) under climate change—range, abundance, genetic diversity and adaptive response. For Ecol Manag 259:2213–2222

    Article  Google Scholar 

  27. 27.

    Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637

    Article  Google Scholar 

  28. 28.

    Davis MB, Shaw RG (2001) Range shifts and adaptive responses to Quaternary climate change. Science 292:673–679

    Article  Google Scholar 

  29. 29.

    Shi PL, Zhang XZ, Zhong ZM et al (2006) Diurnal and seasonal variability of soil CO2 efflux in a cropland ecosystem on the Tibetan Plateau. Agr For Meteorol 137:220–233

    Article  Google Scholar 

  30. 30.

    Liao JJ, Shen GZ, Li YK (2013) Lake variations in response to climate change in the Tibetan Plateau in the past 40 years. Int J Digit Earth 6:534–549

    Article  Google Scholar 

  31. 31.

    Ding MJ, Zhang YL, Sun XM et al (2013) Spatiotemporal variation in alpine grassland phenology in the Qinghai-Tibetan Plateau from 1999 to 2009. Chin Sci Bull 58:396–405

    Article  Google Scholar 

  32. 32.

    Piao SL, Fang JY, He JS (2006) Variations in vegetation net primary production in the Qinghai-Xizang Plateau, China, from 1982 to 1999. Clim Change 74:253–267

    Article  Google Scholar 

  33. 33.

    Lin XW, Zhang ZH, Wang SP et al (2011) Response of ecosystem respiration to warming and grazing during the growing seasons in the alpine meadow on the Tibetan plateau. Agr For Meteorol 151:792–802

    Article  Google Scholar 

  34. 34.

    Saito M, Kato T, Tang YH (2009) Temperature controls ecosystem CO2 exchange of an alpine meadow on the northeastern Tibetan Plateau. Glob Change Biol 15:221–228

    Article  Google Scholar 

  35. 35.

    Piao SL, Cui MD, Chen AP et al (2011) Altitude and temperature dependence of change in the spring vegetation green-up date from 1982 to 2006 in the Qinghai-Xizang Plateau. Agr For Meteorol 151:1599–1608

    Article  Google Scholar 

  36. 36.

    Shen MG, Tang YH, Chen J et al (2011) Influences of temperature and precipitation before the growing season on spring phenology in grasslands of the central and eastern Qinghai-Tibetan Plateau. Agr For Meteorol 151:1711–1722

    Article  Google Scholar 

  37. 37.

    Huete A, Didan K, Miura T et al (2002) Overview of the radiometric and biophysical performance of the MODIS vegetation indices. Remote Sens Environ 83:195–213

    Article  Google Scholar 

  38. 38.

    Ganguly S, Friedl MA, Tan B et al (2010) Land surface phenology from MODIS: characterization of the collection 5 global land cover dynamics product. Remote Sens Environ 114:1805–1816

    Article  Google Scholar 

  39. 39.

    Zhang XY, Friedl MA, Schaaf CB et al (2003) Monitoring vegetation phenology using MODIS. Remote Sens Environ 84:471–475

    Article  Google Scholar 

  40. 40.

    Zhang XS (2007) Vegetation map of the People’s Republic of China 1:1 000 000. The Geological Publishing House, Beijing (in Chinese)

    Google Scholar 

  41. 41.

    Xu WX, Liu XD (2007) Response of vegetation in the Qinghai-Tibet Plateau to global warming. Chin Geogr Sci 17:151–159

    Article  Google Scholar 

  42. 42.

    Farr TG, Rosen PA, Caro E et al (2007) The shuttle radar topography mission. Rev Geophys 45:RG2004

    Article  Google Scholar 

  43. 43.

    Rabus B, Eineder M, Roth A et al (2003) The shuttle radar topography mission—a new class of digital elevation models acquired by spaceborne radar. ISPRS J Photogramm 57:241–262

    Article  Google Scholar 

  44. 44.

    Hijmans RJ, Cameron SE, Parra JL et al (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978

    Article  Google Scholar 

  45. 45.

    Zhang GL, Zhang YJ, Dong JW et al (2013) Green-up dates in the Tibetan Plateau have continuously advanced from 1982 to 2011. Proc Natl Acad Sci USA 110:4309–4314

  46. 46.

    De Beurs KM, Henebry GM (2005) Land surface phenology and temperature variation in the International Geosphere–Biosphere Program high-latitude transects. Glob Change Biol 11:779–790

    Article  Google Scholar 

  47. 47.

    Liang L, Schwartz MD (2013) Testing a growth efficiency hypothesis with continental-scale phenological variations of common and cloned plants. Int J Biometeorol 1–9

  48. 48.

    Chen XQ, Xu L (2012) Phenological responses of Ulmus pumila (Siberian Elm) to climate change in the temperate zone of China. Int J Biometeorol 56:695–706

    Article  Google Scholar 

  49. 49.

    Zhang XY, Tarpley D, Sullivan JT (2007) Diverse responses of vegetation phenology to a warming climate. Geophys Res Lett 34:L19405

    Article  Google Scholar 

  50. 50.

    Vitasse Y, Delzon S, Bresson CC et al (2009) Altitudinal differentiation in growth and phenology among populations of temperate-zone tree species growing in a common garden. Can J For Res 39:1259–1269

    Article  Google Scholar 

  51. 51.

    Wang YF, Li XX, Dawadi B et al (2013) Phenological variation in height growth and needle unfolding of Smith fir along an altitudinal gradient on the southeastern Tibetan Plateau. Trees 27:401–407

    Article  Google Scholar 

  52. 52.

    Montague J, Barrett S, Eckert C (2008) Re-establishment of clinal variation in flowering time among introduced populations of purple loosestrife (Lythrum salicaria, Lythraceae). J Evol Biol 21:234–245

    Google Scholar 

  53. 53.

    Li HT, Wang XL, Hamann A (2010) Genetic adaptation of aspen (Populus tremuloides) populations to spring risk environments: a novel remote sensing approach. Can J For Res 40:2082–2090

    Article  Google Scholar 

  54. 54.

    Liu LL, Liu LY, Hu Y (2012) Response of spring phenology to climate change across Tibetan Plateau. In: 2012 2nd International Conference on Remote Sensing, Environment and Transportation Engineering (RSETE 2012), Nanjing, June 2012. IEEE, Piscataway, NJ, USA

  55. 55.

    Wang WY, Wang QJ, Wang HC (2006) The effect of land management on plant community composition, species diversity, and productivity of alpine Kobersia steppe meadow. Ecol Res 21:181–187

    Article  Google Scholar 

  56. 56.

    Wang CT, Cao GM, Wang QL et al (2008) Changes in plant biomass and species composition of alpine Kobresia meadows along altitudinal gradient on the Qinghai-Tibetan Plateau. Sci China Ser C Life Sci 51:86–94

    Article  Google Scholar 

  57. 57.

    Craine JM, Wolkovich EM, Towne E (2012) The roles of shifting and filtering in generating community-level flowering phenology. Ecography 35:1033–1038

    Article  Google Scholar 

  58. 58.

    IPCC2007. Climate Change 2007: The Physical Science Basis: Summary for Policymakers. Intergovernmental Panel on Climate Change, Geneva, Switzerland

  59. 59.

    Richardson AD, Hollinger DY, Dail DB et al (2009) Influence of spring phenology on seasonal and annual carbon balance in two contrasting New England forests. Tree Physiol 29:321–331

    Article  Google Scholar 

  60. 60.

    Dragoni D, Schmid HP, Wayson CA et al (2011) Evidence of increased net ecosystem productivity associated with a longer vegetated season in a deciduous forest in south-central Indiana, USA. Glob Change Biol 17:886–897

    Article  Google Scholar 

  61. 61.

    Cannell M, Smith R (1983) Thermal time, chill days and prediction of budburst in Picea sitchensis. J Appl Ecol 20:951–963

    Article  Google Scholar 

  62. 62.

    Inouye DW (2008) Effects of climate change on phenology, frost damage, and floral abundance of montane wildflowers. Ecology 89:353–362

    Article  Google Scholar 

  63. 63.

    Thomson JD (2010) Flowering phenology, fruiting success and progressive deterioration of pollination in an early-flowering geophyte. Philos T Roy Soc B 365:3187–3199

    Article  Google Scholar 

  64. 64.

    Aldridge G, Inouye DW, Forrest JR et al (2011) Emergence of a mid-season period of low floral resources in a montane meadow ecosystem associated with climate change. J Ecol 99:905–913

    Article  Google Scholar 

  65. 65.

    Willis CG, Ruhfel BR, Primack RB et al (2010) Favorable climate change response explains non-native species’ success in Thoreau’s woods. PLoS One 5:e8878

Download references


This work was supported by the National Basic Research Program (CB951701), the External Cooperation Program of the Chinese Academy of Sciences (GJH21123), and the National Natural Science Foundation of China (40971197). We also thank CIAT for providing DEM data and Haiying Yu for useful comments.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information



Corresponding author

Correspondence to Liangyun Liu.

About this article

Verify currency and authenticity via CrossMark

Cite this article

Liu, L., Liu, L., Liang, L. et al. Effects of elevation on spring phenological sensitivity to temperature in Tibetan Plateau grasslands. Chin. Sci. Bull. 59, 4856–4863 (2014). https://doi.org/10.1007/s11434-014-0476-2

Download citation


  • Temperature sensitivity
  • Elevation
  • Growth efficiency
  • Land surface phenology
  • Greenup
  • Grasslands