Skip to main content

Advertisement

SpringerLink
Log in

Phenological changes in herbaceous plants in China’s grasslands and their responses to climate change: a meta-analysis

  • Original Paper
  • Published:
International Journal of Biometeorology Aims and scope Submit manuscript

Abstract

Plant phenological events are sensitive indicators of climate change, and their change could markedly affect the structure and function of ecosystems. Previous studies have revealed the spatiotemporal variations in the phenological events of woody plants. However, limited studies have focused on the phenophases of herbaceous plants. In this study, by using a meta-analysis method, we extracted information about the phenological changes in herbaceous plants in China’s grasslands from existing studies (including the period, station, species, phenophases, phenological trends, and climatic determinants) and analyzed the patterns manifested in the dataset. The results showed that the spring phenophases (e.g., first leaf date and first flowering date) of the herbaceous plants mainly advanced over the past 30 years, but a large difference existed across grassland types. The spring phenophases of forages (species from the Cyperaceae, Gramineae, and Leguminosae families) became earlier in the desert steppe and alpine steppe but showed no apparent trends in the alpine meadow and even became later in the meadow steppe and typical steppe. In most cases, the increase in spring temperatures and precipitation promoted the greening up of herbaceous plants, while sunshine duration was positively correlated with the green-up date of herbaceous plants. For the autumn phenophases, the proportions of the earlier and later trends were very close, but the trends varied among the grassland types. The leaf coloring dates of the forages were delayed in the meadow steppe and alpine steppe but showed no distinct pattern in the typical steppe or alpine meadow and even became earlier in the desert steppe. In most cases, the increase in growing season temperature led to an earlier leaf coloring date of the herbaceous plants, but the increase in the preseason precipitation delayed the leaf coloring date. Our results suggested that the phenophases of herbaceous plants have complicated responses to multiple environmental factors, which makes predicting future phenological changes difficult.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Bahuguna RN, Jagadish KSV (2015) Temperature regulation of plant phenological development. Environ Exp Bot 111:83–90

    CAS  Google Scholar 

  • Bolmgren K, Vanhoenacker D, Miller-Rushing AJ (2013) One man, 73 years, and 25 species. Evaluating phenological responses using a lifelong study of first flowering dates. Int J Biometeorol 57(3):367–375

    CAS  Google Scholar 

  • Chen X, Li Q (2009) Relationships between Leymus chinensis phenology and meteorological factors in Inner Mongolia grasslands. Acta Ecol Sin 29(10):5280–5290 (in Chinese)

    Google Scholar 

  • Cheng M, Jin J, Zhang J, Jiang H, Wang R (2018) Effect of climate change on vegetation phenology of different land-cover types on the Tibetan Plateau. Int J Remote Sens 39(2):470–487

    Google Scholar 

  • Cleland EE, Chuine I, Menzel A, Mooney HA, Schwartz MD (2007) Shifting plant phenology in response to global change. Trends Ecol Evol 22(7):365

    Google Scholar 

  • Dai J, Wang H, Ge Q (2013) Multiple phenological responses to climate change among 42 plant species in Xi’an, China. Int J Biometeorol 57(5):749–758

    Google Scholar 

  • Fu YH, Zhao H, Piao S (2015) Declining global warming effects on the phenology of spring leaf unfolding. Nature. 526(7571):104–107

    CAS  Google Scholar 

  • Gao Y (2018) Effect of climate change on the phenological phase of herbs in meadow grassland of Tongliao City, InnerMongolia. Pratacult Sci 35(2):423–433 (in Chinese)

    Google Scholar 

  • Ge Q, Wang H, Rutishauser T, Dai J (2015) Phenological response to climate change in China: a meta-analysis. Glob Chang Biol 21(1):265–274

    Google Scholar 

  • Gong Z, Kawamura K, Ishikawa N, Goto M, Wulan T, Alateng D, Yin T, Ito Y (2015) MODIS normalized difference vegetation index (NDVI) and vegetation phenology dynamics in the Inner Mongolia grassland. Solid Earth 6(4):1185–1194

    Google Scholar 

  • Gu R, Zhou W, Bai M, Li X, Di R, Yang J (2012) Impacts of climate change on phenological phase of herb in the main grassland in Inner Mongolia. Acta Ecol Sin 32(03):767–776 (in Chinese)

    Google Scholar 

  • Guan K, Wood EF, Medvigy D, Kimball J, Pan M, Caylor KK, Sheffield J, Xu X, Jones MO (2014) Terrestrial hydrological controls on land surface phenology of African savannas and woodlands. J Geophys Res-Biogeo 119(8):1652–1669

    Google Scholar 

  • Guo Q, Li S, Hu Z, Zhao W, Yu G, Sun X, Li L, Liang N, Bai W (2016) Responses of gross primary productivity to different sizes of precipitation events in a temperate grassland ecosystem in Inner Mongolia, China. J Arid Land 8(1):36–46

    Google Scholar 

  • Han F, Zhang Q, Buyantuev A, Niu J, Liu PT, Li XH, Kang S, Zhang J, Chang CM, Li YP (2015) Effects of climate change on phenology and primary productivity in the desert steppe of Inner Mongolia. J Arid Land 7(2):251–263

    Google Scholar 

  • Hou X, Gao S, Niu Z, Xu Z (2014) Extracting grassland vegetation phenology in North China based on cumulative SPOT-VEGETATION NDVI data. Int J Remote Sens 35(9):3316–3330

    Google Scholar 

  • Hu Q, Pan F, Pan X, Zhang D, Li Q, Pan Z, Wei Y (2015) Spatial analysis of climate change in Inner Mongolia during 1961–2012. China Appl Geogr 60:254–260

    Google Scholar 

  • Huang W, Ge Q, Wang H, Dai J (2019) Effects of multiple climate change factors on the spring phenology of herbaceous plants in Inner Mongolia, China: evidence from ground observation and controlled experiments. Int J Climatol 39(13):5140–5153

    Google Scholar 

  • IPCC (2013) Summary for policymakers. In: Stocker TF, Qin D, Plattner GK, Tignor M, Allen SK, Boschung J et al (eds) Climate Change 2013: The physical science basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, pp 3–29

    Google Scholar 

  • IPCC (2014) Summary for policymakers. In: Field CB, Barros VR, Dokken DJ, Mach KJ, Mastrandrea MD, Bilir TE et al (eds) Climate change 2014: impacts, adaptation, and vulnerability. Part A: global and sectoral aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, pp 1–32

    Google Scholar 

  • John R, Chen J, Lu N, Wilske B (2009) Land cover/land use change in semi-arid Inner Mongolia: 1992-2004. Environ Res Lett 4(4):45010

    Google Scholar 

  • Kenneth KE, Easterling DR, Redmond K, Hubbard K (2003) Temporal variations of extreme precipitation events in the United States: 1895–2000. Geophys Res Lett 30(17):1–7

    Google Scholar 

  • Lamarque P, Lavorel S, Mouchet M, Quetier F (2014) Plant trait-based models identify direct and indirect effects of climate change on bundles of grassland ecosystem services. Proc Natl Acad Sci U S A 111(38):13751–13756

    CAS  Google Scholar 

  • Lesica P, Kittelson PM (2010) Precipitation and temperature are associated with advanced flowering phenology in a semi-arid grassland. J Arid Environ 74(9):1013–1017

    Google Scholar 

  • Li X, Han G (2013) Response of grass growing season to meteorological change in eastern Inner Mongolia grassland. Chin J Ecol 32(04):987–992 (in Chinese)

    Google Scholar 

  • Li S, Verburg PH, Lv S, Wu J, Li X (2012) Spatial analysis of the driving factors of grassland degradation under conditions of climate change and intensive use in Inner Mongolia, China. Reg Environ Chang 12(3):461–474

    Google Scholar 

  • Li X, Guo C, Han G (2013) Impacts of climate change on phenological phases of dominant grass species in the desert steppe in Inner Mongolia. Ecol Environ Sci 22(1):50–57 (in Chinese)

    CAS  Google Scholar 

  • Liang L, Schwartz MD, Fei S (2011) Validating satellite phenology through intensive ground observation and landscape scaling in a mixed seasonal forest. Remote Sens Environ 115(1):143–157

    Google Scholar 

  • Liu H, Tian F, Hu HC, Hu HP, Sivapalan M (2013) Soil moisture controls on patterns of grass green-up in Inner Mongolia: an index based approach. Hydrol Earth Syst Sci 17(2):805–815

    Google Scholar 

  • Liu H, Dong P, Ioannou MS, Li L, Shea J, Pasolli HA, Grimm JB, Rivlin PK, Lavis LD, Koyama M, Liu Z (2018) Visualizing long-term single-molecule dynamics in vivo by stochastic protein labeling. Proc Natl Acad Sci U S A 115(2):343–348

    CAS  Google Scholar 

  • Liu K, Liang T, Qiang W, Du G et al (2020) Changes in seed germination strategy along the successional gradient from abandoned cropland to climax grassland in a subalpine meadow and some implications for rangeland restoration. Agric Ecosyst Environ 289:106746

    Google Scholar 

  • Marcel VO, Gianni B, Mats H (2018) Effects of climate change on grassland biodiversity and productivity: the need for a diversity of models. Agronomy. 8(142):14

    Google Scholar 

  • Menzel A, Sparks TH, Estrella N, Koch E et al (2006) European phenological response to climate change matches the warming pattern. Glob Chang Biol 12(10):1969–1976

    Google Scholar 

  • Miao L, Müller D, Cui X, Ma M (2017) Changes in vegetation phenology on the Mongolian Plateau and their climatic determinants. PLoS One 12(12):e190313

    Google Scholar 

  • Mittler R, Finka A, Goloubinoff P (2012) How do plants feel the heat? Trends Biochem Sci 37(3):118–125

    CAS  Google Scholar 

  • Mokhtari A, Noory H, Vazifedoust M (2018) Performance of different surface incoming solar radiation models and their impacts on reference evapotranspiration. Water Resour Manag 32:3053–3070

    Google Scholar 

  • Munson SM, Long AL (2017) Climate drives shifts in grass reproductive phenology across the western USA. New Phytol 213(4):1945–1955

    Google Scholar 

  • Orlandi F, Ruga L, Bonofiglio T, Romano B (2014) Fifteen-year phenological plant species and meteorological trends in Central Italy. Int J Biometeorol 58(5):661–667

    CAS  Google Scholar 

  • Ren S, Yi S, Peichl M, Wang X (2018) Diverse responses of vegetation phenology to climate change in different grasslands in Inner Mongolia during 2000–2016. Remote Sens-Basel 10(1):17

    Google Scholar 

  • Richardson AD, Keenan TF, Migliavacca M, Ryu Y, Sonnentag O, Toomey M (2013) Climate change, phenology, and phenological control of vegetation feedbacks to the climate system. Agric For Meteorol 169:156–173

    Google Scholar 

  • Sandra L, Karl G, Pénélope L, Pascale CM et al (2011) Using plant functional traits to understand the landscape distribution of multiple ecosystem services. J Ecol 99(1):135–147

    Google Scholar 

  • Sha Z, Zhong J, Bai Y, Tan X, Li J (2016) Spatio-temporal patterns of satellite-derived grassland vegetation phenology from 1998 to 2012 in Inner Mongolia, China. J Arid Land. 8(3):462–477

    Google Scholar 

  • Shi G (2014) Effects of climate change on phenophase of forage grass in Xilinguole typical grassland. Chin Agric Sci Bull 30(29):197–204 (in Chinese)

    Google Scholar 

  • Shi G, Ji X, Chen S (2017) Effects of climate change on phenophase and yield of Cleistogenes squarrosa in Xillinguole typical grassland. Chin J Grassl 39(1):42–49 (in Chinese)

    Google Scholar 

  • Shinoda M, Ito S, Nachinshonhor GU, Erdenetsetseg D (2007) Phenology of Mongolian grasslands and moisture conditions. J Meteorol Soc Jpn 85(3):359–367

    Google Scholar 

  • Sparks TH, Mizera T, Wojtowicz W, Tryjanowski P (2012) Synchrony in the phenology of a culturally iconic spring flower. Int J Biometeorol 56(2):407–409

    Google Scholar 

  • Su X, Wu Y, Dong S, Wen L, Li Y, Wang X (2015) Effects of grassland degradation and re-vegetation on carbon and nitrogen storage in the soils of the headwater area nature reserve on the Qinghai-Tibetan Plateau, China. J Mt Sci-Engl 12(3):582–591

    Google Scholar 

  • Suttie JM, Reynolds SG, Batello C (2005) Grasslands of the world. Food and Agriculture Organization of the United Nations, Rome

    Google Scholar 

  • Tao Z, Wang H, Liu Y, Xu Y, Dai J (2017a) Phenological response of different vegetation types to temperature and precipitation variations in northern China during 1982–2012. Int J Remote Sens 38(11):3236–3252

    Google Scholar 

  • Tao Z, Zhong S, Ge Q, Dai J, Xu Y, Wang H (2017b) Spatiotemporal variations in flowering duration of woody plants in China from 1963 to 2012. Acta Geograph Sin 72(1):53–63 (in Chinese)

    Google Scholar 

  • Tao Z, Huang W, Wang H (2020) Soil moisture outweighs temperature for triggering the green-up date in temperate grasslands. Theor Appl Climatol 140(3):1093–1105

    Google Scholar 

  • Trenberth KE, Fasullo JT, Kiehl J (2009) Earth’s global energy budget. Bull Am Meteorol Soc 90(3):311–323

    Google Scholar 

  • Wang H, Zhong S, Tao Z, Dai J, Ge Q (2017a) Changes in flowering phenology of woody plants from 1963 to 2014 in North China. Int J Biometeorol 63(5):579–590

    CAS  Google Scholar 

  • Wang L, Ning Z, Wang H, Ge Q (2017b) Impact of climate variability on flowering phenology and its implications for the schedule of blossom festivals. Sustainability-Basel. 9(7):1127

    Google Scholar 

  • Wang G, Huang Y, Wei Y, Zhang W, Li T, Zhang Q (2019) Inner Mongolian grassland plant phenological changes and their climatic drivers. Sci Total Environ 683:1–8

    CAS  Google Scholar 

  • Wang H, Liu H, Cao G, Ma Z, Li Y, Zhang F, Zhao X, Zhao X, Jiang L, Sanders NJ, Classen AT, He JS (2020) Alpine grassland plants grow earlier and faster but biomass remains unchanged over 35 years of climate change. Ecol Lett 23(4):701–710

    Google Scholar 

  • Wilsey BJ, Martin LM, Kaul AD (2018) Phenology differences between native and novel exotic-dominated grasslands rival the effects of climate change. J Appl Ecol 55(2):863–873

    Google Scholar 

  • Wittich K, Liedtke M (2015) Shifts in plant phenology: a look at the sensitivity of seasonal phenophases to temperature in Germany. Int J Climatol 35(13):3991–4000

    Google Scholar 

  • Wittmer MHOM, Auerswald K, Bai Y, Schaeufele R, Schnyder H (2010) Changes in the abundance of C3/C4 species of Inner Mongolia grassland: evidence from isotopic composition of soil and vegetation. Glob Chang Biol 16(2):605–616

    Google Scholar 

  • Wu X, Guo S, Yin J, Yang G, Zhong Y, Liu D (2018) On the event-based extreme precipitation across China: time distribution patterns, trends, and return levels. J Hydrol 562:305–317

    Google Scholar 

  • Yang X, Zhao Y, Na R (2010) Phenological characteristics of typical grassland plants in Inner Mongolia and their response to climate change. Inner Mong Pratacult 22(3):51–56 (in Chinese)

    CAS  Google Scholar 

  • Yu FF, Price KP, Ellis J, Shi PJ (2003) Response of seasonal vegetation development to climatic variations in eastern Central Asia. Remote Sens Environ 87(1):42–54

    Google Scholar 

  • Zhang X (2007) Vegetation map of the People’s Republic of China (1:10000000). Geological Publishing House, Beijing

    Google Scholar 

  • Zhang Y, Parazoo NC, Williams AP, Zhou S, Gentine P (2020) Large and projected strengthening moisture limitation on end-of-season photosynthesis. Proc Natl Acad Sci 117(17):9216–9222

    CAS  Google Scholar 

  • Zhong SY, Ge QS, Dai JH, Wang HJ (2017) Development of phenological models for simulating past flowering phenology of typical ornamental plants in China. Resour Sci 39(11):2116–2129 (in Chinese)

    Google Scholar 

  • Zhou Y, Jia G (2016) Precipitation as a control of vegetation phenology for temperate steppes in China. Atmos Ocean Sci Lett 9(3):162–168

    Google Scholar 

Download references

Funding

This research was supported by the National Key R&D Program of China (Grant No. 2016YFC0503304 and 2018YFA0606102) and National Natural Science Foundation of China (Grant No. 41771056).

Author information

Authors and Affiliations

  1. State Key Laboratory of Environmental Criteria and Risk Assessment, Chinese Research Academy of Environmental Sciences, Beijing, 100012, China

    Wenjie Huang, Wei Wang, Junsheng Li, Chunting Feng & Jinhong Du

  2. Key Laboratory of Land Surface Pattern and Simulation, Institute of Geographic Sciences and Natural Resources Research, Chinese Academy of Sciences, Beijing, 100101, China

    Junhu Dai

Authors
  1. Wenjie Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Junhu Dai
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wei Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Junsheng Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chunting Feng
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jinhong Du
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Wei Wang or Junsheng Li.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 202 kb)

ESM 2

(XLS 160 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Huang, W., Dai, J., Wang, W. et al. Phenological changes in herbaceous plants in China’s grasslands and their responses to climate change: a meta-analysis. Int J Biometeorol 64, 1865–1876 (2020). https://doi.org/10.1007/s00484-020-01974-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00484-020-01974-1

Keywords

Search

Navigation