Chin J Plan Ecolo ›› 2018, Vol. 42 ›› Issue (1): 20-27.doi: 10.17521/cjpe.2017.0133

• Research Articles • Previous Articles     Next Articles

Experimental warming changed plants’ phenological sequences of two dominant species in an alpine meadow, western of Sichuan

ZHANG Li1,2,WANG Gen-Xu1,RAN Fei1,PENG A-Hui1,2,XIAO Yao1,2,YANG Yang1,YANG Yan1,*()   

  1. 1 Institute of Mountain Hazards and Environment, Chinese Academy of Sciences, Chengdu 610041, China

    2 University of Chinese Academy of Sciences, Beijing 100049, China
  • Online:2018-01-18 Published:2018-01-20
  • Contact: Yan YANG
  • Supported by:
    Supported by the Key Research Program of Frontier Sciences, Chinese Academy of Sciences(QYZDJ-SSW-DQC006);the National Key Research and Development Project of China(2017YFC0504900);the National Natural Science Foundation of China(31100323);the National Natural Science Foundation of China(31300416)


Aims We studied phenological sequences of two dominant plants (Polygonum viviparum and Potentilla leuconota) in an alpine meadow of the Hengduan Mt., western of Sichuan to explore the alpine plants responses on climate change.

Methods Open-top chambers (OTCs) chosen by ITEX were used to monitor the warming in the field. After a four-year experimental warming, in the 5th growing season we recorded the phenological sequences of two dominant species, focusing on plant responses on warming. The sequence was divided into four stages: budding, flowering, withering and ripe seeds. Each stage had three events: first, peak, and last.

Important findings Our results showed that: 1) For P. viviparum, experimental warming elicited a shortening of the duration of each stage, advanced all of the phenological events but the first of withering and ripe seeds, shortened the period of each stage and reduced the duration of entire reproduction. 2) For P. leuconota, experimental warming extended the duration of every stage. All phenological events before the end of withering occurred earlier on experimental warming but the peak of flowering. The period of each stage had inconsistent responses on warming and warming prolonged the duration of entire reproduction. The present results indicated that not all phenological events were equally responsive to experimental warming and an entire sequence could be a more accurate way to evaluate the responses on environmental variation. Therefore, the plastic responses to warming of different species would have effects on community composition and structure.

Key words: alpine meadow, climate change, open-top chamber, Polygonum viviparum, Potentilla leuconota, reproductive phenology

Fig. 1

Monthly mean air temperature, soil temperature, and soil water content inside and outside the open-top chambers during the growing season. A, Monthly mean air temperature. B, Monthly mean soil temperature at 5 cm soil depth. C, Monthly mean soil temperature at 20 cm soil depth. D, Monthly mean soil water content at 5 cm soil depth. E, Monthly mean soil water content at 20 cm soil depth."

Fig. 2

Phenological shifts at the sequence of Polygonum viviparum (A) and Potentilla leuconota (B). ■, ▲ and ● symbol represent a phenological shift of first, peak, and last of the four stages, respectively. Negative value represents earlier stations than control in days, and the positive value represents delayed stations than control in days. OTCs, open-top chambers."

Table 1

Parameter estimates of GLME models investigating phenological sequences responses to experimental warming"

Potentilla leuconota
Polygonum viviparum
N 截距
OTCs N 截距
开始 First 6 5.11*** -0.03 13 5.19*** 0.01
峰值 Peak 6 5.17 *** -0.05 13 5.19*** 0.01
结束 Last 6 5.23*** -0.01 13 5.28*** 0.02
开始 First 8 5.17*** -0.06 10 5.28*** -0.02
峰值 Peak 8 5.18*** 0.02 10 5.30*** -0.01
结束 Last 8 5.27*** -0.02 10 5.33*** -0.02
开始 First 8 5.18*** -0.05 13 5.25*** 0.02
峰值 Peak 8 5.27 *** -0.03 13 5.30*** 0.01
结束 Last 8 5.36 *** 0.04 13 5.33*** 0.01
Ripe seeds
开始 First 8 5.23*** 0.02 12 5.36*** -0.02
峰值 Peak 8 5.37 *** 0.02 12 5.38*** -0.02
结束 Last 8 5.47*** 0.01 12 5.41*** -0.03

Fig. 3

Effects of open-top chambers (OTCs) warming on the duration of each stage of Polygonum viviparum (A) and Potentilla leuconota (B)(mean ± SE)."

Fig. 4

Effects of open-top chambers (OTCs) warming on the period between the peak time of the neighboring stages of Polygonum viviparum (A) and Potentilla leuconota (B) (mean ± SE)."

Appendix I

Changes in coverage and height of the two species under experimental warming (mean ± SE). *, p < 0.05"

[1] Amano T, Smithers RJ, Sparks TH, Sutherland WJ ( 2010). A 250-year index of first flowering dates and its response to temperature changes. Proceedings of the Royal Society of London B: Biological Sciences, 277, 2451-2457.
doi: 10.1098/rspb.2010.0291 pmid: 20375052
[2] Arft A, Walker M, Gurevitch J, Alatalo J, Bret-Harte M, Dale M, Diemer M, Gugerli F, Henry G, Jones M ( 1999). Responses of tundra plants to experimental warming: Meta-analysis of the international tundra experiment. Ecological Monographs, 69, 491-511.
doi: 10.1890/0012-9615(1999)069[0491:ROTPTE]2.0.CO;2
[3] Badeck FW, Bondeau A, B?ttcher K, Doktor D, Lucht W, Schaber J, Sitch S ( 2004). Responses of spring phenology to climate change. New Phytologist, 162, 295-309.
doi: 10.1111/j.1469-8137.2004.01059.x
[4] Beaubien E, Freeland H ( 2000). Spring phenology trends in Alberta, Canada: Links to ocean temperature. International Journal of Biometeorology, 44, 53-59.
doi: 10.1007/s004840000050 pmid: 10993558
[5] CaraDonna PJ, Iler AM, Inouye DW ( 2014). Shifts in flowering phenology reshape a subalpine plant community. Proceedings of the National Academy of Sciences of the United States of America, 111, 4916-4921.
doi: 10.1073/pnas.1323073111
[6] 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, 13740-13744.
doi: 10.1073/pnas.0600815103 pmid: 16954189
[7] Ding YH, Wang HJ ( 2015). Newly acquired knowledge on the scientific issues related to climate change over the recent 100 years in China. Chinese Science Bulletin, 61, 1029-1041.
[ 丁一汇, 王会军 ( 2015). 近百年中国气候变化科学问题的新认识. 科学通报, 61, 1029-1041.]
[8] Dorji T, Totland ?, Moe SR, Hopping KA, Pan J, 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.
doi: 10.1111/gcb.12059 pmid: 23504784
[9] Dudgeon SR, Steneck RS, Davison IR, Vadas RL ( 1999). Coexistence of similar species in a space-limited intertidal zone. Ecological Monographs, 69, 331-352.
doi: 10.1890/0012-9615(1999)069[0331:COSSIA]2.0.CO;2
[10] Forrest J, Miller-Rushing AJ ( 2010). Toward a synthetic understanding of the role of phenology in ecology and evolution. The Royal Society, 365, 3101-3112.
doi: 10.1098/rstb.2010.0145 pmid: 2981948
[11] Gugger S, Kesselring H, Stocklin J, Hamann E ( 2015). Lower plasticity exhibited by high-versus mid-elevation species in their phenological responses to manipulated temperature and drought. Annals of Botany, 116, 953-962.
doi: 10.1093/aob/mcv155 pmid: 4640129
[12] Hollister RD, Webber PJ, Bay C ( 2005). Plant response to temperature in northern Alaska: Implications for predicting vegetation change. Ecology, 86, 1562-1570.
doi: 10.1890/04-0520
[13] Iler AM, H?ye TT, Inouye DW, Schmidt NM ( 2013). Nonlinear flowering responses to climate: Are species approaching their limits of phenological change? Philosophical Transactions of the Royal Society of London B: Biological Sciences, 368, 20120489, doi: 10.1098/rstb.2012.0489.
doi: 10.1098/rstb.2012.0489 pmid: 3720060
[14] Inouye DW ( 2008). Effects of climate change on phenology, frost damage, and floral abundance of montane wildflowers. Ecology, 89, 353-362.
doi: 10.1890/06-2128.1
[15] IPCC (Intergovernmental Panel on Climate Change) ( 2013) : Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on climate change. In: Stocker TF, Qin DH, Plattner GK, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM eds. Climate Change in 2013: The Physical Science Basis. Cambridge University Press, Cambridge, UK.
[16] Jonasson S, Havstr?m M, Jensen M, Callaghan TV ( 1993). In situ mineralization of nitrogen and phosphorus of arctic soils after perturbations simulating climate change. Oecologia, 95, 179-186.
[17] Klein JA, Harte J, Zhao XQ ( 2004). Experimental warming causes large and rapid species loss, dampened by simulated grazing, on the Tibetan Plateau. Ecology Letters, 7, 1170-1179.
doi: 10.1111/j.1461-0248.2004.00677.x
[18] Li ZX, He YQ, Xin HJ, Wang CF, Jia WX, Zhang W, Liu J ( 2010). Spatio-temporal variations of temperature and precipitation in Mts. Hengduan Region during 1960-2008. Acta Geographica Sinica, 65, 563-579.
doi: 10.11821/xb201005006
[ 李宗省, 何元庆, 辛惠娟, 王春凤, 贾文雄, 张蔚, 刘婧 ( 2010). 我国横断山区1960-2008年气温和降水时空变化特征. 地理学报, 65, 563-579.]
doi: 10.11821/xb201005006
[19] Liu YZ, Reich PB, Li GY, Sun SC ( 2011). Shifting phenology and abundance under experimental warming alters trophic relationships and plant reproductive capacity. Ecology, 92, 1201-1207.
doi: 10.1890/10-2060.1
[20] Memmott J, Craze PG, Waser NM, Price MV ( 2007). Global warming and the disruption of plant-pollinator interactions. Ecology Letters, 10, 710-717.
doi: 10.1111/ele.2007.10.issue-8
[21] Meng FD, Cui SJ, Wang SP, Duan JC, Jiang LL, Zhang ZH, Luo CY, Wang Q, Zhou Y, Li XN, Zhang LR, Dorji T, Li YN, Du MY, Wang GJ ( 2016). Changes in phenological sequences of alpine communities across a natural elevation gradient. Agricultural and Forest Meteorology, 224, 11-16.
doi: 10.1016/j.agrformet.2016.04.013
[22] Menzel A, Sparks TH, Estrella N, Koch E, Aasa A, Ahas R, Alm-Kubler K, Bissolli P, Braslavská O, Briede A ( 2006). European phenological response to climate change matches the warming pattern. Global Change Biology, 12, 1969-1976.
doi: 10.1053/jlts.2003.50055
[23] Pe?uelas J, Filella I ( 2001). Responses to a warming world. Science, 294, 793-795.
doi: 10.1126/science.1066860 pmid: 11679652
[24] Pe?uelas J, Filella I ( 2009). Phenology feedbacks on climate change. Science, 324, 887-888.
doi: 10.1126/science.1173004 pmid: 19443770
[25] Pe?uelas J, Filella I, Comas P ( 2002). Changed plant and animal life cycles from 1952 to 2000 in the Mediterranean region. Global Change Biology, 8, 531-544.
doi: 10.1046/j.1365-2486.2002.00489.x
[26] Pepin N, Bradley RS, Diaz HF, Baraer M, Caceres EB, Forsythe N, Fowler H, Greenwood G, Hashmi MZ, Liu XD, Miller JR, Ning L, Ohmura A, Palazzi E, Rangwala I, Sch?ner W, Severskiy I, Shahgedanova M, Wang MB, Williamson SN, Yang DQ ( 2015). Elevation-dependent warming in mountain regions of the world. Nature Climate Change, 5, 424-430.
doi: 10.1038/nclimate2563
[27] Post ES, Pedersen C, Wilmers CC, Forchhammer MC ( 2008). Phenological sequences reveal aggregate life history response to climatic warming. Ecology, 89, 363-370.
doi: 10.1890/06-2138.1
[28] Price MV, Waser NM ( 1998). Effects of experimental warming on plant reproductive phenology in a subalpine meadow. Ecology, 79, 1261-1271.
doi: 10.1890/0012-9658(1998)079[1261:EOEWOP]2.0.CO;2
[29] Root TL, Price JT, Hall KR, Schneider SH, Rosenzweig C, Pounds JA ( 2003). Fingerprints of global warming on wild animals and plants. Nature, 421, 57-60.
doi: 10.1038/nature01333 pmid: 12511952
[30] Schwartz MD, Reiter BE ( 2000). Changes in North American spring. International Journal of Climatology, 20, 929-932.
doi: 10.1002/1097-0088(20000630)20:83.0.CO;2-5
[31] Thomas CD, Cameron A, Green RE, Bakkenes M, Beaumont LJ, Collingham YC, Erasmus BF, de Siqueira MF, Grainger A, Hannah L ( 2004). Extinction risk from climate change. Nature, 427, 145-148.
doi: 10.1038/nature02121 pmid: 14712274
[32] Tilman D, Lehman CL, Thomson KT ( 1997). Plant diversity and ecosystem productivity: Theoretical considerations. Proceedings of the National Academy of Sciences of the United States of America, 94, 1857-1861.
doi: 10.1073/pnas.94.5.1857 pmid: 11038606
[33] Totland ?, Schulte-Herbrüggen B ( 2003). Breeding system, insect flower visitation, and floral traits of two alpine Cerastium species in Norway. Arctic, Antarctic, and Alpine Research, 35, 242-247.
[34] Wang SP, Meng FD, Duan JC, Wang YF, Cui XY, Piao SL, Niu HS, Xu GP, Luo CY, Zhang ZH ( 2014). Asymmetric sensitivity of first flowering date to warming and cooling in alpine plants. Ecology, 95, 3387-3398.
doi: 10.1890/13-2235.1
[35] Wolkovich EM, Cook BI, Allen JM, Crimmins TM, Betancourt JL, Travers SE, Pau S, Regetz J, Davies TJ, Kraft NJ ( 2012). Warming experiments under predict plant phenological responses to climate change. Nature, 485, 494-497.
doi: 10.1038/nature11014 pmid: 22622576
[36] Yang Y, Wang GX, Klanderud K, Wang JF, Liu GS ( 2015). Plant community responses to five years of simulated climate warming in an alpine fen of the Qinghai-Tibetan Plateau. Plant Ecology & Diversity, 8, 211-218.
doi: 10.1080/17550874.2013.871654
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[1] Zhu Chen;Liu Fei-yan and Zeng Guang-wen. Effects of 4PU on the Senescence of Detached Radish Cotyledons[J]. Chin Bull Bot, 1997, 14(04): 42 -44 .
[2] FU Hong CHI Zhe-Ru① CHANG Jie FU Cheng-Xin. Extraction of Leaf Vein Features Based on Artificial Neural Network — Studies on the Living Plant Identification Ⅰ[J]. Chin Bull Bot, 2004, 21(04): 429 -436 .
[3] Hongyan Li;Qingsong Zheng;Zhaopu Liu*;Qing Li. Effects of Various Concentration of Seawater on the Growth and Physiological Characteristics of Lactuca indica Seedlings[J]. Chin Bull Bot, 2010, 45(01): 73 -78 .
[4] . [J]. Chin Bull Bot, 1994, 11(专辑): 10 .
[5] YANG Jia-Ju YI Tie-Mei ZHAO Cai-yun. Nomenclature and Identification of Gymnosperm Fossil Woods in China[J]. Chin Bull Bot, 2000, 17(专辑): 117 -129 .
[6] Yan Liu, Lijing Xing, Junhua Li, Shaojun Dai. Rice B-box Zinc Finger Protein OsBBX25 is Involved in the Abiotic Response[J]. Chin Bull Bot, 2012, 47(4): 366 -378 .
[7] Qiaoling Zhu, Jiayi Leng, Qingsheng Ye. Photosynthetic Characteristics of Dendrobium williamsonii and D. longicornu[J]. Chin Bull Bot, 2013, 48(2): 151 -159 .
[8] . [J]. Chin J Plan Ecolo, 1963, (1): 110 -130 .
[9] Fan Zheng, Hu Shizhi. Report of the 1st National Scientific and Working Conference on the Classification, Regionalization and Mapping of Vegetation[J]. Chin J Plan Ecolo, 1981, 5(2): 147 -148 .