Welcome to Journal of University of Chinese Academy of Sciences,Today is

Effects of climate changes on plant phenology at high-latitude and alpine regions

  • MENG Fandong ,
  • ZHOU Yang ,
  • CUI Shujuan ,
  • WANG Qi ,
  • TSECHOE Dorji ,
  • WANG Shiping
Expand
  • 1. Key Laboratory of Alpine Ecology and Biodiversity, Institute of Tibetan Plateau Research, Chinese Academy of Sciences, Beijing 100101, China;
    2. CAS Center for Excellence in Tibetan Plateau Earth Science, Beijing 100101, China;
    3. University of Chinese Academy of Sciences, Beijing 100049, China

Received date: 2016-06-03

  Revised date: 2017-02-20

  Online published: 2017-07-15

Abstract

Phenology studies the timing of periodic phenomena of biological events, which is affected by biotic and abiotic factors. We review the main influences of climatic factors (e.g., temperature, precipitation, and timing of snowmelt) and species on plant phenology at high-latitude and alpine regions. Most previous studies indicated that warming and earlier snowmelt advanced green-up and first flowering but delayed senescence of individuals and community. The effects of precipitation on plant phenology were inconsistent. There were few studies on root phenology, and no general conclusions were obtained. Root phenology was affected by changes in soil temperature, moisture, and nutrient availability. The divergent responses found in magnitude and direction were mainly due to different measurements, sites, species, and ecosystems. Therefore, long-term ground observations of individuals and community phenological sequences are needed in order to deeply understand the processes and mechanisms of the effects of biotic and abiotic factors in the future. Ground observations of community phenology are particularly needed at high-latitude and alpine areas to match with remote sensing methods and scale from local site to large landscape. Furthermore, root phenology and biological mechanisms of phenological responses to climate changes should be studied.

Cite this article

MENG Fandong , ZHOU Yang , CUI Shujuan , WANG Qi , TSECHOE Dorji , WANG Shiping . Effects of climate changes on plant phenology at high-latitude and alpine regions[J]. Journal of University of Chinese Academy of Sciences, 2017 , 34(4) : 498 -507 . DOI: 10.7523/j.issn.2095-6134.2017.04.012

References

[1] Lieth H. Phenology and seasonality modeling [M]. New York: Springer Science and Business Media, 2013: 4-19.
[2] Walther G R, Post E, Convey P, et al. Ecological responses to recent climate change [J]. Nature, 2002, 416(6 879): 389-395.
[3] Cleland E E, Chuine I, Menzel A, et al. Shifting plant phenology in response to global change [J]. Trends in Ecology & Evolution, 2007, 22(7): 357-365.
[4] Richardson A D, Keenan T F, Migliavacca M, et al. Climate change, phenology, and phenological control of vegetation feedbacks to the climate system [J]. Agricultural and Forest Meteorology, 2013, 169(2 013): 156-173.
[5] Kathuroju N, White M A, Symanzik J, et al. On the use of the advanced very high resolution radiometer for development of prognostic land surface phenology models [J]. Ecological Modelling, 2007, 201(2): 144-156.
[6] Wang S, Wang C, Duan J, et al. Timing and duration of phenological sequences of alpine plants along an elevation gradient on the Tibetan plateau [J]. Agricultural and Forest Meteorology, 2014, 189/190(2 014): 220-228.
[7] Wang S, Meng F, Duan J, et al. Asymmetric sensitivity of first flowering date to warming and cooling in alpine plants [J]. Ecology, 2014, 95(12): 3 387-3 398.
[8] Dorji T, Totland O, Moe S R, et al. Plant functional traits mediate reproductive phenology and success in response to experimental warming and snow addition in Tibet [J]. Global Change Biology, 2013, 19(2): 459-472.
[9] Piao S, Cui M, Chen A, et al. Altitude and temperature dependence of change in the spring vegetation green-up date from 1982 to 2006 in the Qinghai-Xizang Plateau [J]. Agricultural and Forest Meteorology, 2011, 151(12): 1 599-1 608.
[10] Jeong S, Ho C, Gim H, et al. Phenology shifts at start vs. end of growing season in temperate vegetation over the Northern Hemisphere for the period 1982-2008 [J]. Global Change Biology, 2011, 17(7): 2 385-2 399.
[11] Chuine I, Yiou P, Viovy N, et al. Historical phenology: grape ripening as a past climate indicator [J]. Nature, 2004, 432(7 015): 289-290.
[12] Lambert A M, Miller-Rushing A J, Inouye D W. Changes in snowmelt date and summer precipitation affect the flowering phenology of Erythronium grandiflorum (glacier lily; liliaceae) [J]. American Journal of Botany, 2010, 97(9): 1 431-1 437.
[13] Hansen J, Sato M, Ruedy R, et al. Global temperature change [J]. Proceedings of the National Academy of Sciences, 2006, 103(39): 14 288-14 293.
[14] Houghton J T, Ding Y, Griggs D J, et al. Climate Change 2001: The scientific basis [M]. Cambridge: The Press Syndicate of Cambridge University, 2001: 156-159.
[15] Thomas C D, Cameron A, Green R E, et al. Extinction risk from climate change [J]. Nature, 2004, 427(6 970): 145-148.
[16] Inouye D W, Wielgolaski F E. Phenology at High Altitudes [C]//Schwartz M D. Phenology: An integrative environmental science. London, UK: Kluwer Academic, 2013: 249-272.
[17] Wolkovich E M, Cook B I, Allen J M, et al. Warming experiments underpredict plant phenological responses to climate change [J]. Nature, 2012, 485(7 399): 494-497.
[18] Ibanez I, Primack R B, Miller-Rushing A J, et al. Forecasting phenology under global warming [J]. Philosophical Transactions of the Royal Society B-Biological Sciences, 2010, 365(1 555): 3 247-3 260.
[19] Walker M D, Wahren C H, Hollister R D, et al. Plant community responses to experimental warming across the tundra biome [J]. Proceedings of the National Academy of Sciences USA, 2006, 103(5): 1342-1346.
[20] Forrest J, Inouye D W, Thomson J D. Flowering phenology in subalpine meadows: Does climate variation influence community co-flowering patterns? [J]. Ecology, 2010, 91(2): 431-440.
[21] Bliss L. Adaptations of arctic and alpine plants to environmental conditions [J]. Arctic, 1962, 15(2): 117-144.
[22] Tieszen L L, Lewis M C, Miller P C, et al. An analysis of processes of primary production in tundra growth forms [C]//Bliss L C, Heal O W, Moore J J. Tundra ecosystems: a comparative analysis. New York, USA: Cambridge University Press, 1981: 285-356.
[23] Pieper S J, Loewen V, Gill M, et al. Plant responses to natural and experimental variations in temperature in alpine tundra, southern Yukon, Canada [J]. Arctic, Antarctic, and Alpine Research, 2011, 43(3): 442-456.
[24] 葛全胜, 戴君虎, 郑景云. 物候学研究进展及中国现代物候学面临的挑战 [J]. 中国科学院院刊, 2010, 25(3): 310-316.
[25] Wielgolaski F E, Inouye D W. Phenology at High Latitudes [C]//Schwartz M D. Phenology: an integrative environmental science. London, UK: Kluwer Academic, 2013: 225-247.
[26] Keller F, Körner C. The role of photoperiodism in alpine plant development [J]. Arctic, Antarctic, and Alpine Research, 2003, 35(3): 361-368.
[27] Jiang L, Wang S, Meng F, et al. Relatively stable response of fruiting stage to warming and cooling relative to other phenological events [J]. Ecology, 2016, 97(8): 1 961-1 969.
[28] Wang K, Zhang L, Qiu Y, et al. Snow effects on alpine vegetation in the Qinghai-Tibetan Plateau [J]. International Journal of Digital Earth, 2015, 8(1): 56-73.
[29] Arft A M, Walker M D, Gurevitch J, et al. Responses of tundra plants to experimental warming: meta-analysis of the international tundra experiment [J]. Ecological Monographs, 1999, 69(4): 491-511.
[30] Delbart N, Picard G. Modeling the date of leaf appearance in low-arctic tundra [J]. Global Change Biology, 2007, 13(12): 2 551-2 562.
[31] Miller-Rushing A J, Primack R B. Global warming and flowering times in Thoreau's Concord: a community perspective[J]. Ecology, 2008, 89(2): 332-341.
[32] Sherry R A, Zhou X, Gu S, et al. Divergence of reproductive phenology under climate warming [J]. Proceedings of the National Academy of Sciences USA, 2007, 104(1): 198-202.
[33] Meng F, Cui S, Wang S, et al. Changes in phenological sequences of alpine communities across a natural elevation gradient [J]. Agricultural and Forest Meteorology, 2016, 224(2 016): 11-16.
[34] Defila C, Clot B. Phytophenological trends in the Swiss Alps, 1951-2002 [J]. Meteorologische Zeitschrift, 2005, 14(2): 191-196.
[35] Xu Z, Hu T, Wang K, et al. Short-term responses of phenology, shoot growth and leaf traits of four alpine shrubs in a timberline ecotone to simulated global warming, Eastern Tibetan Plateau, China [J]. Plant Species Biology, 2009, 24(1): 27-34.
[36] Hart R, Salick J, Ranjitkar S, et al. Herbarium specimens show contrasting phenological responses to Himalayan climate [J]. Proceedings of the National Academy of Sciences USA, 2014, 111(29): 10 615-10 619.
[37] Cook B I, Wolkovich E M, Parmesan C. Divergent responses to spring and winter warming drive community level flowering trends [J]. Proceedings of the National Academy of Sciences USA, 2012, 109(23): 9 000-9 005.
[38] Post E S, Pedersen C, Wilmers C C, et al. Phenological sequences reveal aggregate life history response to climatic warming [J]. Ecology, 2008, 89(2): 363-370.
[39] CaraDonna P J, Iler A M, Inouye D W. Shifts in flowering phenology reshape a subalpine plant community [J]. Proceedings of the National Academy of Sciences USA, 2014, 111(13): 4 916-4 921.
[40] Stearns S C. The evolution of life histories [M]. Davies, CA, USA: Oxford University Press Oxford, 1992: 230-250.
[41] Taeger S, Sparks T H, Menzel A. Effects of temperature and drought manipulations on seedlings of Scots pine provenances [J]. Plant biology (Stuttgart, Germany), 2015, 17(2): 361-372.
[42] Peñuelas J, Filella I, Zhang X, et al. Complex spatiotemporal phenological shifts as a response to rainfall changes [J]. New Phytologist, 2004, 161(3): 837-846.
[43] Galen C. Why do flowers vary? [J]. Bioscience, 1999, 49(8): 631.
[44] 吕新苗, 康世昌,朱立平, 等. 西藏纳木错植物物候及其对气候的响应 [J]. 山地学报, 2009, 27(6): 648-654.
[45] Reyes-Fox M, Steltzer H, Trlica M J, et al. Elevated CO2 further lengthens growing season under warming conditions [J]. Nature, 2014, 510(7 504): 259-262.
[46] White A, Cannell M G, Friend A D. Climate change impacts on ecosystems and the terrestrial carbon sink: a new assessment [J]. Global environmental change, 1999, 9(1 999): S21-S30.
[47] Beniston M, Diaz H, Bradley R. Climatic change at high elevation sites: an overview [J]. Climatic Change, 1997, 36 (3/4): 233-251.
[48] Yu Z, Liu S, Wang J, et al. Effects of seasonal snow on the growing season of temperate vegetation in China [J]. Global Change Biology, 2013, 19(7): 2 182-2 195.
[49] Odland A. Estimation of the growing season length in alpine areas: effects of snow and temperatures [C]//Scmidt J G. Alpine environment: geology, ecology and conservation. New York: Nova Science Publication, 2011: 1-50.
[50] Woodley E J, Svoboda J. Effects of habitat on variations of phenology and nutrient concentration among four common plant species of the Alexandra Fiord Lowland [C]//Svoboda J, Freedman B. Ecology of a polar oasis, Alexandra Fiord, Ellesmere Island, Canada. Toronto: Captus University Press, 1994: 157-175.
[51] Nobrega S, Grogan P. Deeper snow enhances winter respiration from both plant-associated and bulk soil carbon pools in birch hummock tundra [J]. Ecosystems, 2007, 10(3): 419-431.
[52] Shutova E, Wielgolaski F E, Karlsen S R, et al. Growing seasons of Nordic mountain birch in northernmost Europe as indicated by long-term field studies and analyses of satellite images [J]. International Journal of Biometeorology, 2006, 51(2): 155-166.
[53] Larcher W. Klimastreβ im Gebirge: adaptation straining und Selektionsfilter für Pflanzen. Florengeschichte im Spiegel blütenökologischer Erkenntnisse [M]. German: VS Verlag für Sozialwissenschaften, 1980:49-80.
[54] Körner C. Alpine plant life: Functional plant ecology of high mountain ecosystems [M]. New York, USA: Springer Science & Business Media, 2003: 40-41.
[55] Stinson K A. Natural selection favors rapid reproductive phenology in Potentilla pulcherrima (Rosaceae) at opposite ends of a subalpine snowmelt gradient [J]. American Journal of Botany, 2004, 91(4): 531-539.
[56] Ernakovich J G, Hopping K A, Berdanier A B, et al. Predicted responses of arctic and alpine ecosystems to altered seasonality under climate change [J]. Global Change Biology, 2014, 20(10): 3 256-3 269.
[57] Meng F, Zhou Y, Wang S, et al. Temperature sensitivity thresholds to warming and cooling in phenophases of alpine plants [J]. Climatic Change, 2016, 239(2 016): 579-590.
[58] Yu H, Luedeling E, Xu J. Winter and spring warming result in delayed spring phenology on the Tibetan Plateau [J]. Proceedings of the National Academy of Sciences USA, 2010, 107(51): 22 151-22 156.
[59] Shen M, Sun Z, Wang S, et al. No evidence of continuously advanced green-up dates in the Tibetan Plateau over the last decade [J]. Proceedings of the National Academy of Sciences USA, 2013, 110(26): E2 329.
[60] Yi S, Zhou Z. Increasing contamination might have delayed spring phenology on the Tibetan Plateau [J]. Proceedings of the National Academy of Sciences USA, 2011, 108(19): E94-E94.
[61] Chen H, Zhu Q, Wu N, et al. Delayed spring phenology on the Tibetan Plateau may also be attributable to other factors than winter and spring warming [J]. Proceedings of the National Academy of Sciences USA, 2011, 108(19): E93.
[62] Marchand F L, Nijs I, Heuer M, et al. Climate warming postpones senescence in High Arctic tundra [J]. Arctic Antarctic and Alpine Research, 2004, 36(4): 390-394.
[63] Zavaleta E S, Thomas B D, Chiariello N R, et al. Plants reverse warming effect on ecosystem water balance [J]. Proceedings of the National Academy of Sciences, 2003, 100(17): 9 892-9 893.
[64] Morin X, Roy J, Sonie L, et al. Changes in leaf phenology of three European oak species in response to experimental climate change [J]. New Phytologist, 2010, 186(4): 900-910.
[65] Craine J M, Wolkovich E M, Towne E G, et al. Flowering phenology as a functional trait in a tallgrass prairie [J]. New Phytologist, 2012, 193(3): 673-682.
[66] Kliber A, Eckert C G. Sequential decline in allocation among flowers within inflorescences: Proximate mechanisms and adaptive significance [J]. Ecology, 2004, 85(6): 1 675-1 687.
[67] Memmott J, Craze P G, Waser N M, et al. Global warming and the disruption of plant-pollinator interactions [J]. Ecology Letters, 2007, 10(8): 710-717.
[68] Cleland E E, Chiariello N R, Loarie S R, et al. Diverse responses of phenology to global changes in a grassland ecosystem [J]. Proceedings of the National Academy of Sciences USA, 2006, 103(37): 13 740-13 744.
[69] 裴顺祥, 郭泉水, 辛学兵, 等. 国外植物物候对气候变化响应的研究进展 [J]. 世界林业研究, 2009, 22(6): 31-37.
[70] Shen M, Tang Y, Chen J, et al. Influences of temperature and precipitation before the growing season on spring phenology in grasslands of the central and eastern Qinghai-Tibetan Plateau [J]. Agricultural and Forest Meteorology, 2011, 151(12): 1 711-1 722.
[71] Robinson D. Implications of a large global root biomass for carbon sink estimates and for soil carbon dynamics [J]. Proceedings of the Royal Society B: Biological, Sciences, 2007, 274(1 626): 2 753-2 759.
[72] Brouwer R.Functional equilibrium: sense or nonsense [J].Netherlands Journal of Agricultural Science, 1983, 31(4): 335-348.
[73] Radville L, McCormack M L, Post E, et al. Root phenology in a changing climate [J]. Journal of Experimental Botany, 2016, 67(12): 3 617-3 628.
[74] Blume-Werry G, Wilson S D, Kreyling J, et al. The hidden season: growing season is 50% longer below than above ground along an arctic elevation gradient [J]. New Phytologist, 2016, 209(3): 978-986.
[75] Sullivan P F, Welker J M. Warming chambers stimulate early season growth of an arctic sedge: Results of a minirhizotron field study [J]. Oecologia, 2005, 142(4): 616-626.
[76] Steinaker D F, Wilson S D, Peltzer D A. Asynchronicity in root and shoot phenology in grasses and woody plants [J]. Global Change Biology, 2010, 16(8): 2 241-2 251.
[77] Tierney G L, Fahey T J, Groffman P M, et al. Environmental control of fine root dynamics in a northern hardwood forest [J]. Global Change Biology, 2003, 9(5): 670-679.
[78] Najar A, Landhausser S M, Whitehill J G, et al. Reserves accumulated in non-photosynthetic organs during the previous growing season drive plant defenses and growth in aspen in the subsequent growing season [J]. Journal of Chemical Ecology, 2014, 40(1): 21-30.
[79] Kummerow J, Russell M. Seasonal root-growth in the Arctic tussock tundra [J]. Oecologia, 1980, 47(2): 196-199.
[80] Edwards E J, Benham D G, Marland L A, et al. Root production is determined by radiation flux in a temperate grassland community [J]. Global Change Biology, 2004, 10(2): 209-227.
[81] McCormack M L, Adams T S, Smithwick E A H, et al. Variability in root production, phenology, and turnover rate among 12 temperate tree species [J]. Ecology, 2014, 95(8): 2 224-2 235.
[82] Romberger J A, Mikola P. International Review of Forestry Research [M]. New York & London: Academic press, 1967: 181-206.
[83] Eissenstat D M, Caldwell M M. Competitive ability is linked to rates of water extraction: a field study of 2 aridland tussock grasses [J]. Oecologia, 1988, 75(1): 1-7.
[84] Hendrick R L, Pregitzer K S. The relationship between fine root demography and the soil environment in northern hardwood forests [J]. Ecoscience, 1997, 4(1): 99-105.
[85] 龙毅, 孟凡栋, 王常顺, 等. 高寒草甸主要植物地上地下生物量分布及退化对根冠比和根系表面积的影响 [J]. 广西植物, 2015, 35(4): 532-538.
[86] Hendrick R L, Pregitzer K S. Temporal and depth-related patterns of fine root dynamics in northern hardwood forests [J]. Journal of Ecology, 1996, 84(2): 167-176.
[87] Blume-Werry G, Wilson S D, Kreyling J, et al. The hidden season: growing season is 50% longer below than above ground along an arctic elevation gradient [J]. New Phytologist, 2016, 209(3): 978-986.
[88] Onipchenko V G, Makarov M I, van Logtestijn R S, et al. New nitrogen uptake strategy: specialized snow roots [J]. Ecology Letters, 2009, 12(8): 758-764.
[89] Tierney G L, Fahey T J, Groffman P M, et al. Soil freezing alters fine root dynamics in a northern hardwood forest [J]. Biogeochemistry, 2001, 56(2): 175-190.
[90] Shaver G R, Billings W D. Effects of daylength and temperature on root elongation in tundra-graminoids [J]. Oecologia, 1977, 28(1): 57-65.
[91] Steltzer H, Post E. Seasons and life cycles [J]. Science, 2009, 324 (5 929): 886-887.
[92] Xia J, Wan S. Independent effects of warming and nitrogen addition on plant phenology in the Inner Mongolian steppe [J]. Annals of Botany, 2013, 111(6): 1 207-1 217.
[93] Wang S, Duan J, Xu G, et al. Effects of warming and grazing on soil N availability, species composition, and ANPP in an alpine meadow [J]. Ecology, 2012, 93(11): 2 365-2 376.
[94] Meng F, Jiang L, Zhang Z, et al., Changes in flowering functional group affect responses of community phenological sequences to temperature change [J]. Ecology, 2016, DOI: 10.1002/ecy.1685.
[95] Tang J, Körner C, Muraoka H, et al. Emerging opportunities and challenges in phenology: a review [J]. Ecosphere, 2016, DOI: 10.1002/ecs2.1436.
[96] Fenner M. The phenology of growth and reproduction in plants: perspectives in plant ecology [J]. Evolution and Systematics, 1998, 1(1):78-91.
[97] Rutishauser T, Stockli R, Harte J, et al. Climate change: flowering in the greenhouse [J]. Nature, 2012, 485(7 399): 448-449.
[98] 王力, 李凤霞, 周万福,等. 气候变化对不同海拔高山嵩草物候期的影响[J]. 草业科学,2012, 29(8): 1 256-1 261.
[99] Diez J M, Ibanez I, Miller-Rushing A J, et al. Forecasting phenology: from species variability to community patterns [J]. Ecology Letters, 2012, 15(6): 545-553.
[100] Iler A M, Hoye T T, Inouye D W, et al. Nonlinear flowering responses to climate: Are species approaching their limits of phenological change? [J]. Philosophical Transactions of the Royal Society B-Biological Sciences, 2013, 368(1 624): 20 120 489.
[101] Cornelius C, Estrella N, Franz H, et al. Linking altitudinal gradients and temperature responses of plant phenology in the Bavarian Alps [J]. Plant Biology, 2013, 15(2 013): 57-69.
[102] Ganjurjav H, Gao Q, Schwartz M W, et al. Complex responses of spring vegetation growth to climate in a moisture-limited alpine meadow [J]. Scientific Reports, 2016, 6: 23 356.
Outlines

/