Effects of experimental warming on plant reproductive phenology in Xizang alpine meadow

ZHU Jun-Tao1

(1.Lhasa Plateau Ecosystem Research Station, Key Laboratory of Ecosystem Network Observation and Modeling, Institute of Geographic Sciences and Natural Resources Research, Chinese Academy of Sciences, Beijing, China 100101)

【Abstract】 Aims Climate warming strongly influences the reproductive phenology of plants in alpine and arctic ecosystems. Here we focus on the phenological shifts caused by warming in a typical alpine meadow on the Qinghai-Xizang Plateau. Our objective was to explore the phenological responses of alpine plant species to experimental warming. Methods Passive warming was achieved using open-top chambers (OTCs). The treatments included control (C), and four levels of warming (T1, T2, T3, T4). We selected Kobresia pygmaea, Potentilla saundersiana, Potentilla cuneata, Stipa purpurea, Festuca coelestis and Youngia simulatrix as the focal species. Plant phenology was scored every 3–5 days in the growing season. The reproductive phenology phases of each species were estimated through fitting the phenological scores to the Richards function. Important findings Under soil water stress caused by warming, most plants in the alpine meadow advanced or delayed their reproductive events. As a result, warming significantly delayed the phenological development of K. pygmaea. Warming significantly advanced the reproductive phenology of P. saundersiana, S. purpurea and F. coelestis, but not that of P. cuneata and Y. simulatrix. In addition, warming significantly shortened the average flowering duration of alpine plant species. The potentially warmer and drier growing seasons under climate change may shift the reproductive phenology of the alpine systems in similar pattern.

【Keywords】 alpine meadow; experimental warming; phenological shifts; reproductive phenology; Qinghai-Xizang Plateau;


【Funds】 National Special Science Research Program of China (2013CB956302 and 2010CB950603) National Natural Science Foundation of China (41571195) “West Light” Foundation of the Chinese Academy of Sciences

Download this article


    Ashe XH (2013). Effects of warming and precipitation regime on plant phenology and productivity in an alpine meadow, Northwestern Sichuan, China. Master degree dissertation, Chengdu University of Technology, Chengdu (in Chinese with English abstract).

    Arft AM, Walker MD, Gurevitch J, Alatalo JM, Bret-Harte MS, Dale M (1999). Response patterns of tundra plant species to experimental warming: A meta-analysis of the international tundra experiment. Ecological Monographs, 69, 491–511.

    Bjorkman AD, Elmendorf SC, Beamish AL, Vellend M, Henry GHR (2015). Contrasting effects of warming and increased snowfall on Arctic tundra plant phenology over the past two decades. Global Change Biology, 21, 4651–4661.

    Chmielewski FM, Rötzer T (2001). Response of tree phenology to climate change across Europe. Agricultural and Forest Meteorology, 108, 101–112.

    Cleland EE, Chiariello NR, Loarie SR, Mooney HA, Field CB (2006). Diverse responses of phenology to global changes in a grassland ecosystem. Proceedings of the National Academy of Sciences of the United States of America, 103, 13740.

    Cook BI, Wolkovich EM, Parmesan C (2012). Divergent responses to spring and winter warming drive community level flowering trends. Proceedings of the National Academy of Sciences of the United States of America, 109, 9000–9005.

    Dorji T, Totland Ø, Moe S, Hopping KA, Pan JB, Klein JA (2013). Plant functional traits mediate reproductive phenology and success in response to experimental warming and snow addition in Tibet. Global Change Biology, 19, 459–472.

    Dunne JA, Harte J, Taylor KJ (2003). Subalpine meadow flowering phenology responses to climate change: Integrating experimental and gradient methods. Ecological Monographs, 73, 69–86.

    Fitter AH, Fitter RSR (2002). Rapid changes in flowering time in British plants. Science, 296, 1689–1691.

    Franks SJ, Sim S, Weis AE (2007). Rapid evolution of flowering time by an annual plant in response to a climate fluctuation. Proceedings of the National Academy of Sciences of the United States of America, 104, 1278–1282.

    Goldman DA, Willson MF (1986). Sex allocation in functionally hermaphroditic plants: A review and critique. Botanical Review, 52, 157–194.

    Gu S, Hui D, Bian A (1998). The contraction-expansion algorithm and its use in fitting nonlinear equations. International Journal of Biomathematics, 13, 426–434.

    Hoffmann AA, Camac JS, Williams RJ, Papst W, Jarrad FC, Wahren C-H (2010). Phenological changes in six Australian subalpine plants in response to experimental warming and year-to-year variation. Journal of Ecology, 98, 927–937.

    Hollister RD, Webber PJ, Bay C (2005). Plant response to temperature in northern Alaska: Implications for predicting vegetation change. Ecology, 86, 1562–1570.

    IPCC (Intergovernmental Panel on Climate Change) (2007). Contribution of working group Ⅰ to the fourth assessment report of the intergovernmental panel on climate change. In: Solomon S, Qin DH, Manning M, Marquis M, Chen ZL, Averyt K, Tignor M, Miller HL eds. Climate Change2007: The Physical Science Basis. Cambridge University Press, Cambridge, UK.

    Klein JA, Harte J, Zhao XQ (2008). Decline in medicinal and forage species with warming is mediated by plant traits on the Tibetan Plateau. Ecosystems, 11, 775–789.

    Kliber A, Eckert CG (2004). Sequential decline in allocation among flowers within inflorescences: Proximate mechanism and adaptive significance. Ecology, 85, 1675–1687.

    Li YH, Han GD, Wang Z, Zhao ML, Wang ZW, Zhao HB (2014). Influences of warming and nitrogen addition on plant reproductive phenology in Inner Mongolia desert steppe. Chinese Journal of Ecology, 33, 849–856 (in Chinese with English abstract).

    Piao SL, Fang JY, Zhou LM, Philippe C, Zhu B (2006). Variations in satellite-derived phenology in China’s temperate vegetation. Global Change Biology, 12, 672–685.

    Porporato A, Laio F, Ridolfi L, Rodriguez-Iturbe I (2001). Plants in water-controlled ecosystems: Active role in hydrologic processes and response to water stress: Ⅲ. Vegetation water stress. Advances in Water Resources, 24, 725–744.

    Post ES, Pedersen C, Wilmers CC, Forchhammer MC (2008). Phenological sequences reveal aggregate life history response to climatic warming. Ecology, 89, 363–370.

    Price MV, Waser NM (1998). Effects of experimental warming on plant reproductive phenology in a subalpine meadow. Ecology, 79, 1261–1271.

    Richards FJ (1959). A flexible growth function for empirical use. Journal of Experimental Botany, 10, 290–301.

    Rutishauser T, Stockli R, Harte J, Kueppers L (2012). Climate change: Flowering in the greenhouse. Nature, 485, 448–449.

    Sherry RA, Zhou XH, Gu SL, Arnone JA, Schimel DS, Verburg PS, Wallace LL, Luo YQ (2007). Divergence of reproductive phenology under climate warming. Proceedings of the National Academy of Sciences of the United States of America, 104, 198–202.

    Springate DA, Kover PX (2014). Plant responses to elevated temperatures: A field study on phenological sensitivity and fitness responses to simulated climate warming. Global Change Biology, 20, 456–465.

    Visser ME, Both C (2005). Shifts in phenology due to global climate change: The need for a yardstick. Proceedings of the Royal Society Biological Sciences, 272, 2561–2569.

    Wang SP, Meng FD, Duan JC, Wang YF, Cui XY, Piao SL, Niu HS, Xu GP, Luo CY, Zhang ZH, Zhu XX, Shen MG, Li YN, Du MY, Tang YH, Zhao XQ, Ciais PB, Kimball B, Peñuelas J, Janssens IA, Cui SJ, Zhao L, Zhang FW (2014). Asymmetric sensitivity of first flowering date to warming and cooling in alpine plants. Ecology, 95, 3387–3398.

    Wolkovich EM, Cook BI, Allen JM, Crimmins TM, Betancourt JL, Travers SE, Pau S, Regetz J, Davies TJ, Kraft NJB, Ault TR, Bolmgren K, Mazer SJ, Mc Cabe GJ, Mc Gill BJ, Parmesan C, Salamin N, Schwartz MD, Cleland EE (2012). Warming experiments underpredict plant phenological responses to climate change. Nature, 485, 494–497.

    Xia J, Wan S (2013). Independent effects of warming and nitrogen addition on plant phenology in the Inner Mongolian steppe. Annals of Botany, 111, 1207–1217.

    Yu H, Luedeling E, Xu J (2010). Winter and spring warming result in delayed spring phenology on the Tibetan Plateau. Proceedings of the National Academy of Sciences of the United States of America, 107, 22151–22156.

This Article



Vol 40, No. 10, Pages 1028-1036

October 2016


Article Outline


  • 1 Materials and methods
  • 2 Results
  • 3 Discussion
  • References