Plant and Soil

, Volume 425, Issue 1–2, pp 177–188 | Cite as

Early-spring soil warming partially offsets the enhancement of alpine grassland aboveground productivity induced by warmer growing seasons on the Qinghai-Tibetan Plateau

  • Liang Guo
  • Ji Chen
  • Eike Luedeling
  • Jin-Sheng He
  • Jimin Cheng
  • Zhongming Wen
  • Changhui PengEmail author
Regular Article



The response of vegetation productivity to global warming is becoming a worldwide concern. While most reports on responses to warming trends are based on measured increases in air temperature, few studies have evaluated long-term variation in soil temperature and its impacts on vegetation productivity. Such impacts are especially important for high-latitude or high-altitude regions, where low temperature is recognized as the most critical limitation for plant growth.


We used Partial Least Squares regression to correlate long-term aboveground net primary productivity (ANPP) data of an alpine grassland on the Qinghai-Tibetan Plateau with daily air and soil temperatures during 1997–2011. We also analyzed temporal trends for air temperature and soil temperature at different depths.


Soil temperatures have steadily increased at a rate of 0.4–0.9 °C per decade, whereas air temperatures showed no significant trend between 1997 and 2011. While temperature increases during the growing season (May–August) promoted aboveground productivity, warming before the growing season (March–April) had a negative effect on productivity. The negative effect was amplified in the soil layers, especially at 15 cm depth, where variation in aboveground productivity was dominated by early-spring soil warming, rather than by increasing temperature during the growing season.


Future warming, especially in winter and spring, may further reduce soil water availability in early spring, which may slow down or even reverse the increases in grassland aboveground productivity that have widely been reported on the Qinghai-Tibetan Plateau.


Aboveground net primary productivity (ANPP) Alpine grassland Climate warming Qinghai-Tibetan Plateau Soil temperature 



We thank the staff at the Haibei Grassland Ecological Monitoring Station on the Qinghai-Tibetan Plateau for collecting grassland aboveground productivity, weather and soil temperature data since 1997. This research was supported by the National Natural Science Foundation of China (41701606 & 41701292), the National Key Research Program of China (2016YFC0500700), the China Postdoctoral Science Foundation (2016 M590974 & 2017M610647), the Natural Science Basic Research Plan in Shaanxi Province (2017JQ3015 & 2017JQ3041), the West Light Foundation of the Chinese Academy of Sciences (K318021507), and the program from Northwest A&F University (2452016108). Further support was supplied by the Key Cultivation Project of the Chinese Academy of Sciences and Fundamental Research Funds for the Central Universities (3102016QD078). We also thank the field editor from Plant and Soil and four anonymous reviewers who provided constructive and thoughtful comments on earlier drafts of this paper.

Compliance with ethical standards

Conflict of interest

The authors have no conflicts of interest or ethical issues to declare.

Supplementary material

11104_2018_3582_MOESM1_ESM.docx (1.5 mb)
ESM 1 (DOCX 1584 kb)


  1. Barnard R, Leadley PW, Hungate BA (2005) Global change, nitrification, and denitrification: a review. Glob Biogeochem Cycles 19:GB1007CrossRefGoogle Scholar
  2. Bollero GA, Bullock DG, Hollinger SE (1996) Soil temperature and planting date effects on corn yield, leaf area, and plant development. Agron J 88:385–390CrossRefGoogle Scholar
  3. Che M, Chen B, Innes JL et al (2014) Spatial and temporal variations in the end date of the vegetation growing season throughout the Qinghai–Tibetan Plateau from 1982 to 2011. Agric For Meteorol 189-190:81–90CrossRefGoogle Scholar
  4. Chen J, Zhou X, Wang J et al (2016) Grazing exclusion reduced soil respiration but increased its temperature sensitivity in a meadow grassland on the Tibetan Plateau. Ecol Evol 6:675–687CrossRefPubMedPubMedCentralGoogle Scholar
  5. Chen W, Zhang Y, Cihlar J, Smith SL, Riseborough DW (2003) Changes in soil temperature and active layer thickness during the twentieth century in a region in western Canada. J Geophys Res Atmos 108:4696CrossRefGoogle Scholar
  6. Cleland EE, Chiariello NR, Loarie SR, Mooney HA, Field CB (2006) Diverse responses of phenology to global changes in a grassland ecosystem. Proc Natl Acad Sci U S A 103:13740–13744CrossRefPubMedPubMedCentralGoogle Scholar
  7. De Boeck HJ, Lemmens CMHM, Zavalloni C et al (2008) Biomass production in experimental grasslands of different species richness during three years of climate warming. Biogeosciences 5:585–594CrossRefGoogle Scholar
  8. Dieleman WI, Vicca S, Dijkstra FA et al (2012) Simple additive effects are rare: a quantitative review of plant biomass and soil process responses to combined manipulations of CO2 and temperature. Glob Chang Biol 18:2681–2693CrossRefPubMedGoogle Scholar
  9. Flanagan LB, Sharp EJ, Letts MG (2013) Response of plant biomass and soil respiration to experimental warming and precipitation manipulation in a Northern Great Plains grassland. Agric For Meteorol 173:40–52CrossRefGoogle Scholar
  10. Fu YH, Zhao H, Piao S et al (2015) Declining global warming effects on the phenology of spring leaf unfolding. Nature 526:104–107CrossRefPubMedGoogle Scholar
  11. Gao Y, Zhou X, Wang Q et al (2013) Vegetation net primary productivity and its response to climate change during 2001–2008 in the Tibetan Plateau. Sci Total Environ 444:356–362CrossRefPubMedGoogle Scholar
  12. García-Suárez AM, Butler CJ (2006) Soil temperatures at Armagh Observatory, Northern Ireland, from 1904 to 2002. Int J Climatol 26:1075–1089CrossRefGoogle Scholar
  13. Geng Y, Baumann F, Song C et al (2017) Increasing temperature reduces the coupling between available nitrogen and phosphorus in soils of Chinese grasslands. Sci Rep 7:43524CrossRefPubMedPubMedCentralGoogle Scholar
  14. Gong S, Zhang T, Guo R, Cao H, Shi L, Guo J, Sun W (2015) Response of soil enzyme activity to warming and nitrogen addition in a meadow steppe. Soil Res 53:242–252CrossRefGoogle Scholar
  15. Han G, Wang Y, Fang S (2011) Climate change over the Qinghai-Tibet Plateau and its impacts on local agriculture and animal husbandry in the last 50 years. Resour Sci 33:1969–1975Google Scholar
  16. Harte J, Shaw R (1995) Shifting dominance within a montane vegetation community: results of a climate-warming experiment. Science 267:876–880CrossRefPubMedGoogle Scholar
  17. Helama S, Tuomenvirta H, Venäläinen A (2011) Boreal and subarctic soils under climatic change. Glob Planet Chang 79:37–47CrossRefGoogle Scholar
  18. Hu Q, Feng S (2003) A daily soil temperature dataset and soil temperature climatology of the contiguous United States. J Appl Meteorol 42:1139–1156CrossRefGoogle Scholar
  19. IPCC (2013) Climate Change 2013: The Physical Science Basis. Working Group I Contribution to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, United Kingdom and New York, NY, USAGoogle Scholar
  20. Isard SA, Schaetzl RJ, Andresen JA (2007) Soils cool as climate warms in the Great Lakes Region: 1951–2000. Ann Assoc Am Geogr 97:467–476CrossRefGoogle Scholar
  21. Jacobs AFG, Heusinkveld BG, Holtslag AAM (2011) Long-term record and analysis of soil temperatures and soil heat fluxes in a grassland area, The Netherlands. Agric For Meteorol 151:774–780CrossRefGoogle Scholar
  22. La Pierre KJ, Yuan S, Chang CC, Avolio ML, Hallett LM, Schreck T, Smith MD (2011) Explaining temporal variation in above-ground productivity in a mesic grassland: the role of climate and flowering. J Ecol 99:1250–1262CrossRefGoogle Scholar
  23. Ladwig LM, Ratajczak ZR, Ocheltree TW et al (2016) Beyond arctic and alpine: the influence of winter climate on temperate ecosystems. Ecology 97:372–382CrossRefPubMedGoogle Scholar
  24. Lucht W, Prentice IC, Myneni RB et al (2002) Climatic control of the high-latitude vegetation greening trend and pinatubo effect. Science 296:1687–1689CrossRefPubMedGoogle Scholar
  25. Luedeling E (2017) chillR: Statistical Methods for Phenology Analysis in Temperate Fruit Trees. R Package Version 0.66.
  26. Luedeling E, Gassner A (2012) Partial Least Squares regression for analyzing walnut phenology in California. Agric For Meteorol 158:43–52CrossRefGoogle Scholar
  27. Luedeling E, Guo L, Dai J, Leslie C, Blanke MM (2013) Differential responses of trees to temperature variation during the chilling and forcing phases. Agric For Meteorol 181:33–42CrossRefGoogle Scholar
  28. Luo Y, Zhou X (2010) Soil Respiration and the Environment. Academic press, San DiegoGoogle Scholar
  29. Melillo JM, Steudler PA, Aber JD et al (2002) Soil warming and carbon-cycle feedbacks to the climate system. Science 298:2173CrossRefPubMedGoogle Scholar
  30. Menzel A, Sparks TH, Estrella N et al (2006) European phenological response to climate change matches the warming pattern. Glob Chang Biol 12:1969–1976CrossRefGoogle Scholar
  31. Mevik BH, Wehrens R, Liland K (2016) PLS: Partial Least Squares and Principal Component Regression. R Package Version 2.6.0.
  32. Nychka D, Furrer R, Paige J, Sain S (2017) Fields: Tools for Spatial Data. R Package Version 9.0.
  33. Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42CrossRefPubMedGoogle Scholar
  34. Piao S, Fang J, He J (2006) Variations in vegetation net primary production in the Qinghai-Xizang Plateau, China, from 1982 to 1999. Clim Chang 74:253–267CrossRefGoogle Scholar
  35. Qian B, Gregorich EG, Gameda S, Hopkins DW, Wang XL (2011) Observed soil temperature trends associated with climate change in Canada. J Geophys Res Atmos 116:D02106Google Scholar
  36. Core Team R (2017) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  37. Rustad L, Campbell J, Marion G et al (2001) A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming. Oecologia 126:543–562CrossRefPubMedGoogle Scholar
  38. Scurlock JMO, Johnson K, Olson RJ (2002) Estimating net primary productivity from grassland biomass dynamics measurements. Glob Chang Biol 8:736–753CrossRefGoogle Scholar
  39. Shen M, Tang Y, Chen J, Zhu X, Zheng Y (2011) Influences of temperature and precipitation before the growing season on spring phenology in grasslands of the central and eastern Qinghai-Tibetan Plateau. Agric For Meteorol 151:1711–1722CrossRefGoogle Scholar
  40. Sun J, Cheng G, Li W (2013) Meta-analysis of relationships between environmental factors and aboveground biomass in the alpine grassland on the Tibetan Plateau. Biogeosciences 10:1707–1715CrossRefGoogle Scholar
  41. Tao F, Yokozawa M, Xu Y, Hayashi Y, Zhang Z (2006) Climate changes and trends in phenology and yields of field crops in China, 1981–2000. Agric For Meteorol 138:82–92CrossRefGoogle Scholar
  42. Wan S, Luo Y, Wallace LL (2002) Changes in microclimate induced by experimental warming and clipping in tallgrass prairie. Glob Chang Biol 8:754–768CrossRefGoogle Scholar
  43. Wold S (1995) PLS for multivariate linear modeling. In: van der Waterbeemd H (ed) Chemometric methods in molecular design: methods and principles in medicinal chemistry. Verlag-Chemie, Weinheim, pp 195–218Google Scholar
  44. Wu Z, Dijkstra P, Koch GW, Hungate BA (2012) Biogeochemical and ecological feedbacks in grassland responses to warming. Nat Clim Chang 2:458–461CrossRefGoogle Scholar
  45. Xu M, Peng F, You Q, Guo J, Tian X, Liu M, Xue X (2015) Effects of warming and clipping on plant and soil properties of an alpine meadow in the Qinghai-Tibetan Plateau, China. J Arid Land 7:189–204CrossRefGoogle Scholar
  46. Xu W, Xin Y, Zhang J, Xiao R, Wang X (2014) Phenological variation of alpine grasses (Gramineae) in the northeastern Qinghai-Tibetan Plateau, China during the last 20 years. Acta Ecol Sin 34:1781–1793CrossRefGoogle Scholar
  47. Yang YH, Fang JY, Pan YD, Ji CJ (2009) Aboveground biomass in Tibetan grasslands. J Arid Environ 73:91–95CrossRefGoogle Scholar
  48. Yu H, Luedeling E, Xu J (2010) Winter and spring warming result in delayed spring phenology on the Tibetan Plateau. Proc Natl Acad Sci U S A 107:22151–22156CrossRefPubMedPubMedCentralGoogle Scholar
  49. Yu H, Xu J, Okuto E, Luedeling E (2012) Seasonal response of grasslands to climate change on the Tibetan Plateau. PLoS One 7:e49230CrossRefPubMedPubMedCentralGoogle Scholar
  50. Zhang G, Zhang Y, Dong J, Xiao X (2013) Green-up dates in the Tibetan Plateau have continuously advanced from 1982 to 2011. Proc Natl Acad Sci U S A 110:4309–4314CrossRefPubMedPubMedCentralGoogle Scholar
  51. Zhang H, Wang E, Zhou D, Luo Z, Zhang Z (2016) Rising soil temperature in China and its potential ecological impact. Sci Rep 6:35530CrossRefPubMedPubMedCentralGoogle Scholar
  52. Zhang T, Barry RG, Gilichinsky D, Bykhovets SS, Sorokovikov VA, Ye J (2001) An amplified signal of climatic change in soil temperatures during the last century at Irkutsk, Russia. Clim Chang 49:41–76CrossRefGoogle Scholar
  53. Zhang Y, Chen W, Smith SL, Riseborough DW, Cihlar J (2005) Soil temperature in Canada during the twentieth century: Complex responses to atmospheric climate change. J Geophys Res Atmos 110:D03112Google Scholar
  54. Zhou L, Tucker CJ, Kaufmann RK, Slayback D, Shabanov NV, Myneni RB (2001) Variations in northern vegetation activity inferred from satellite data of vegetation index during 1981 to 1999. J Geophys Res Atmos 106:20069–20083CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Liang Guo
    • 1
  • Ji Chen
    • 2
    • 3
  • Eike Luedeling
    • 4
    • 5
  • Jin-Sheng He
    • 6
    • 7
  • Jimin Cheng
    • 1
  • Zhongming Wen
    • 1
  • Changhui Peng
    • 1
    • 8
    Email author
  1. 1.State Key Laboratory of Soil Erosion and Dryland Farming on the Loess PlateauNorthwest A&F UniversityYanglingChina
  2. 2.Center for Ecological and Environmental Sciences, Key Laboratory for Space Bioscience & BiotechnologyNorthwestern Polytechnical UniversityXi’anChina
  3. 3.State Key Laboratory of Loess and Quaternary Geology, Institute of Earth EnvironmentChinese Academy of SciencesXi’anChina
  4. 4.University of BonnBonnGermany
  5. 5.World Agroforestry CenterNairobiKenya
  6. 6.Department of Ecology, College of Urban and Environmental SciencesPeking UniversityBeijingChina
  7. 7.Key Laboratory of Adaptation and Evolution of Plateau Biota, Northwest Institute of Plateau BiologyChinese Academy of SciencesXiningChina
  8. 8.Department of Biology Science, Institute of Environment SciencesUniversity of Quebec at MontrealMontrealCanada

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