Skip to main content

Thank you for visiting You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Warming shortens flowering seasons of tundra plant communities


An Author Correction to this article was published on 07 March 2019

This article has been updated


Advancing phenology is one of the most visible effects of climate change on plant communities, and has been especially pronounced in temperature-limited tundra ecosystems. However, phenological responses have been shown to differ greatly between species, with some species shifting phenology more than others. We analysed a database of 42,689 tundra plant phenological observations to show that warmer temperatures are leading to a contraction of community-level flowering seasons in tundra ecosystems due to a greater advancement in the flowering times of late-flowering species than early-flowering species. Shorter flowering seasons with a changing climate have the potential to alter trophic interactions in tundra ecosystems. Interestingly, these findings differ from those of warmer ecosystems, where early-flowering species have been found to be more sensitive to temperature change, suggesting that community-level phenological responses to warming can vary greatly between biomes.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Fig. 1: Conceptual diagram showing how warmer summer temperatures may shorten the length of the flowering season in tundra ecosystems.
Fig. 2: Map of long-term observational and experimental warming studies.
Fig. 3: Temperature sensitivity of FFDs was greater for late- versus early-flowering species.
Fig. 4: The change in FFDs in response to experimental warming was greater for late- versus early-flowering species.
Fig. 5: Warming was related to the change in the duration of the flowering season over time at sites across the tundra biome.

Data availability

The data that support the findings of this study have been archived in the Polar Data Catalogue:

Change history

  • 07 March 2019

    In the version of this Article originally published, the following sentence was missing from the Acknowledgements: “This work was supported by the Norwegian Research Council SnoEco project, grant number 230970”. This text has now been added.


  1. 1.

    Fitter, A. H. & Fitter, R. S. R. Rapid changes in flowering time in British plants. Science 296, 1689–1691 (2002).

    CAS  Article  Google Scholar 

  2. 2.

    Parmesan, C. & Yohe, G. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421, 37–42 (2003).

    CAS  Article  Google Scholar 

  3. 3.

    Thackeray, S. J. et al. Phenological sensitivity to climate across taxa and trophic levels. Nature 535, 241–245 (2016).

    CAS  Article  Google Scholar 

  4. 4.

    Arft, A. M. et al. Responses of tundra plants to experimental warming: meta-analysis of the International Tundra Experiment. Ecol. Monogr. 69, 491–511 (1999).

    Google Scholar 

  5. 5.

    Høye, T. T., Post, E., Meltofte, H., Schmidt, N. M. & Forchhammer, M. C. Rapid advancement of spring in the High Arctic. Curr. Biol. 17, R449–R451 (2007).

    Article  Google Scholar 

  6. 6.

    Parmesan, C. Influences of species, latitudes and methodologies on estimates of phenological response to global warming. Glob. Change Biol. 13, 1860–1872 (2007).

    Article  Google Scholar 

  7. 7.

    Oberbauer, S. F. et al. Phenological response of tundra plants to background climate variation tested using the International Tundra Experiment. Phil. Trans. R. Soc. B 368, 20120481 (2013).

    CAS  Article  Google Scholar 

  8. 8.

    Xu, L. et al. Temperature and vegetation seasonality diminishment over northern lands. Nat. Clim. Change 3, 581–586 (2013).

    Article  Google Scholar 

  9. 9.

    Park, T. et al. Changes in growing season duration and productivity of northern vegetation inferred from long-term remote sensing data. Environ. Res. Lett. 11, 084001 (2016).

    Article  Google Scholar 

  10. 10.

    Xu, C., Liu, H., Williams, A. P., Yin, Y. & Wu, X. Trends toward an earlier peak of the growing season in Northern Hemisphere mid‐latitudes. Glob. Change Biol. 22, 2852–2860 (2016).

    Article  Google Scholar 

  11. 11.

    Bradley, N. L., Leopold, A. C., Ross, J. & Huffaker, W. Phenological changes reflect climate change in Wisconsin. Proc. Natl Acad. Sci. USA 96, 9701–9704 (1999).

    CAS  Article  Google Scholar 

  12. 12.

    Høye, T. T., Post, E., Schmidt, N. M., Trøjelsgaard, K. & Forchhammer, M. C. Shorter flowering seasons and declining abundance of flower visitors in a warmer Arctic. Nat. Clim. Change 3, 759–763 (2013).

    Article  Google Scholar 

  13. 13.

    Bjorkman, A. D., Elmendorf, S. C., Beamish, A. L., Vellend, M. & Henry, G. H. R. Contrasting effects of warming and increased snowfall on Arctic tundra plant phenology over the past two decades. Glob. Change Biol. 21, 4651–4661 (2015).

    Article  Google Scholar 

  14. 14.

    Panchen, Z. A. & Gorelick, R. Flowering and fruiting responses to climate change of two Arctic plant species, purple saxifrage (Saxifraga oppositifolia) and mountain avens (Dryas integrifolia). Arct. Sci. 1, 45–58 (2015).

    Article  Google Scholar 

  15. 15.

    Panchen, Z. A. & Gorelick, R. Prediction of Arctic plant phenological sensitivity to climate change from historical records. Ecol. Evol. 7, 1325–1338 (2017).

    Article  Google Scholar 

  16. 16.

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

    Article  Google Scholar 

  17. 17.

    Dunne, J. A., Harte, J. & Taylor, K. J. Subalpine meadow flowering phenology responses to climate change: integrating experimental and gradient methods. Ecol. Monogr. 73, 69–86 (2003).

    Article  Google Scholar 

  18. 18.

    Menzel, A. et al. European phenological response to climate change matches the warming pattern. Glob. Change Biol. 12, 1969–1976 (2006).

    Article  Google Scholar 

  19. 19.

    Miller-Rushing, A. J. & Inouye, D. W. Variation in the impact of climate change on flowering phenology and abundance: an examination of two pairs of closely related wildflower species. Am. J. Bot. 96, 1821–1829 (2009).

    Article  Google Scholar 

  20. 20.

    Prevéy, J. S. et al. Greater temperature sensitivity of plant phenology at colder sites: implications for convergence across northern latitudes. Glob. Change Biol. 23, 2660–2671 (2017).

    Article  Google Scholar 

  21. 21.

    Shaver, G. R. & Kummerow, J. in Arctic Ecosystems in a Changing Climate: An Ecophysiological Perspective (eds Chapin, F. S., Jefferies, R. L., Reynolds, J. F., Shaver, G. R. & Svoboda, J.) 193–211 (Academic Press, San Diego, 1992).

  22. 22.

    Molau, U. Relationships between flowering phenology and life history strategies in tundra plants. Arct. Alp. Res. 25, 391–402 (1993).

    Article  Google Scholar 

  23. 23.

    Keller, F. & Körner, C. The role of photoperiodism in alpine plant development. Arct. Antarct. Alp. Res. 35, 361–368 (2003).

    Article  Google Scholar 

  24. 24.

    Hollister, R. D., Webber, P. J. & Tweedie, C. E. The response of Alaskan arctic tundra to experimental warming: differences between short- and long-term responses. Glob. Change Biol. 11, 525–536 (2005).

    Article  Google Scholar 

  25. 25.

    Semenchuk, P. R., Elberling, B. & Cooper, E. J. Snow cover and extreme winter warming events control flower abundance of some, but not all species in High Arctic Svalbard. Ecol. Evol. 3, 2586–2599 (2013).

    Article  Google Scholar 

  26. 26.

    Iler, A. M. et al. Maintenance of temporal synchrony between syrphid flies and floral resources despite differential phenological responses to climate. Glob. Change Biol. 19, 2348–2359 (2013).

    Article  Google Scholar 

  27. 27.

    Post, E., Kerby, J., Pedersen, C. & Steltzer, H. Highly individualistic rates of plant phenological advance associated with arctic sea ice dynamics. Biol. Lett. 12, 20160332 (2016).

    Article  Google Scholar 

  28. 28.

    CaraDonna, P. J. & Inouye, D. W. Phenological responses to climate change do not exhibit phylogenetic signal in a subalpine plant community. Ecology 96, 355–361 (2015).

    Article  Google Scholar 

  29. 29.

    Körner, C. & Basler, D. Phenology under global warming. Science 327, 1461–1462 (2010).

    Article  Google Scholar 

  30. 30.

    Cleland, E. E. et al. Phenological tracking enables positive species responses to climate change. Ecology 93, 1765–1771 (2012).

    Article  Google Scholar 

  31. 31.

    Wheeler, H. C., Høye, T. T., Schmidt, N. M., Svenning, J.-C. & Forchhammer, M. C. Phenological mismatch with abiotic conditions—implications for flowering in Arctic plants. Ecology 96, 775–787 (2015).

    Article  Google Scholar 

  32. 32.

    Inouye, D. W. Effects of climate change on phenology, frost damage, and floral abundance of montane wildflowers. Ecology 89, 353–362 (2008).

    Article  Google Scholar 

  33. 33.

    Wipf, S., Stoeckli, V. & Bebi, P. Winter climate change in alpine tundra: plant responses to changes in snow depth and snowmelt timing. Clim. Change 94, 105–121 (2009).

    Article  Google Scholar 

  34. 34.

    Wheeler, J. A. et al. Increased spring freezing vulnerability for alpine shrubs under early snowmelt. Oecologia 175, 219–229 (2014).

    CAS  Article  Google Scholar 

  35. 35.

    Wheeler, J. A. et al. The snow and the willows: earlier spring snowmelt reduces performance in the low-lying alpine shrub Salix herbacea. J. Ecol. 104, 1041–1050 (2016).

    CAS  Article  Google Scholar 

  36. 36.

    Cooper, E. J., Dullinger, S. & Semenchuk, P. Late snowmelt delays plant development and results in lower reproductive success in the High Arctic. Plant Sci. 180, 157–167 (2011).

    CAS  Article  Google Scholar 

  37. 37.

    Parsons, A. N. et al. Growth responses of four sub-Arctic dwarf shrubs to simulated environmental change. J. Ecol. 82, 307–318 (1994).

    Article  Google Scholar 

  38. 38.

    Molau, U., Nordenhäll, U. & Eriksen, B. Onset of flowering and climate variability in an alpine landscape: a 10-year study from Swedish Lapland. Am. J. Bot. 92, 422–431 (2005).

    Article  Google Scholar 

  39. 39.

    Grubb, P. J. The maintenance of species-richness in plant communities: the importance of the regeneration niche. Biol. Rev. 52, 107–145 (1977).

    Article  Google Scholar 

  40. 40.

    Higgins, S. I., Delgado-Cartay, M. D., February, E. C. & Combrink, H. J. Is there a temporal niche separation in the leaf phenology of savanna trees and grasses? J. Biogeogr. 38, 2165–2175 (2011).

    Article  Google Scholar 

  41. 41.

    Sanz-Aguilar, A., Carrete, M., Edelaar, P., Potti, J. & Tella, J. L. The empty temporal niche: breeding phenology differs between coexisting native and invasive birds. Biol. Invasions 17, 3275–3288 (2015).

    Article  Google Scholar 

  42. 42.

    Wolkovich, E. M. & Cleland, E. E. The phenology of plant invasions: a community ecology perspective. Front. Ecol. Environ. 9, 287–294 (2011).

    Article  Google Scholar 

  43. 43.

    Hegland, S. J., Nielsen, A., Lázaro, A. & Bjerknes, A.-L. How does climate warming affect plant–pollinator interactions?. Ecol. Lett. 12, 184–195 (2009).

    Article  Google Scholar 

  44. 44.

    McKinnon, L., Picotin, M., Bolduc, E., Juillet, C. & Bêty, J. Timing of breeding, peak food availability, and effects of mismatch on chick growth in birds nesting in the High Arctic. Can. J. Zool. 90, 961–971 (2012).

    Article  Google Scholar 

  45. 45.

    Kerby, J. T. & Post, E. Advancing plant phenology and reduced herbivore production in a terrestrial system associated with sea ice decline. Nat. Commun. 4, 2514 (2013).

    Article  Google Scholar 

  46. 46.

    Wipf, S. Phenology, growth, and fecundity of eight subarctic tundra species in response to snowmelt manipulations. Plant Ecol. 207, 53–66 (2010).

    Article  Google Scholar 

  47. 47.

    Post, E., Pedersen, C., Wilmers, C. C. & Forchhammer, M. C. Warming, plant phenology and the spatial dimension of trophic mismatch for large herbivores. Proc. R. Soc. B 275, 2005–2013 (2008).

    Article  Google Scholar 

  48. 48.

    Schmidt, N. M. et al. An ecological function in crisis? The temporal overlap between plant flowering and pollinator function shrinks as the Arctic warms. Ecography 39, 1250–1252 (2016).

    Article  Google Scholar 

  49. 49.

    Sherry, R. A. et al. Divergence of reproductive phenology under climate warming. Proc. Natl Acad. Sci. USA 104, 198–202 (2007).

    CAS  Article  Google Scholar 

  50. 50.

    Steltzer, H. & Post, E. Seasons and life cycles. Science 324, 886–887 (2009).

    Article  Google Scholar 

  51. 51.

    Wolkovich, E. M. et al. Warming experiments underpredict plant phenological responses to climate change. Nature 485, 494–497 (2012).

    CAS  Article  Google Scholar 

  52. 52.

    Prevéy, J. S. & Seastedt, T. R. Seasonality of precipitation interacts with exotic species to alter composition and phenology of a semi-arid grassland. J. Ecol. 102, 1549–1561 (2014).

    Article  Google Scholar 

  53. 53.

    Diez, J. M. et al. Forecasting phenology: from species variability to community patterns. Ecol. Lett. 15, 545–553 (2012).

    Article  Google Scholar 

  54. 54.

    Aldridge, G., Inouye, D. W., Forrest, J. R. K., Barr, W. A. & Miller-Rushing, A. J. Emergence of a mid-season period of low floral resources in a montane meadow ecosystem associated with climate change. J. Ecol. 99, 905–913 (2011).

    Article  Google Scholar 

  55. 55.

    CaraDonna, P. J., Iler, A. M. & Inouye, D. W. Shifts in flowering phenology reshape a subalpine plant community. Proc. Natl Acad. Sci. USA 111, 4916–4921 (2014).

    CAS  Article  Google Scholar 

  56. 56.

    Cook, B. I. et al. Sensitivity of spring phenology to warming across temporal and spatial climate gradients in two independent databases. Ecosystems 15, 1283–1294 (2012).

    Article  Google Scholar 

  57. 57.

    Høye, T. T. et al. Phenology of High-Arctic butterflies and their floral resources: species-specific responses to climate change. Curr. Zool. 60, 243–251 (2014).

    Article  Google Scholar 

  58. 58.

    Hocking, B. Insect–flower associations in the High Arctic with special reference to nectar. Oikos 19, 359–387 (1968).

    Article  Google Scholar 

  59. 59.

    Janzen, D. H. Synchronization of sexual reproduction of trees within the dry season in Central America. Evolution 21, 620–637 (1967).

    Article  Google Scholar 

  60. 60.

    Meng, F. D. et al. Changes in flowering functional group affect responses of community phenological sequences to temperature change. Ecology 98, 734–740 (2017).

    CAS  Article  Google Scholar 

  61. 61.

    Hulme, P. E. Contrasting impacts of climate-driven flowering phenology on changes in alien and native plant species distributions. New Phytol. 189, 272–281 (2011).

    Article  Google Scholar 

  62. 62.

    Craine, J. M., Wolkovich, E. M., Gene Towne, E. & Kembel, S. W. Flowering phenology as a functional trait in a tallgrass prairie. New Phytol. 193, 673–682 (2012).

    Article  Google Scholar 

  63. 63.

    Miller-Rushing, A. J., Høye, T. T., Inouye, D. W. & Post, E. The effects of phenological mismatches on demography. Philos. Trans. R. Soc. Lond. B 365, 3177–3186 (2010).

    Article  Google Scholar 

  64. 64.

    Elmendorf, S. C. et al. Experiment, monitoring, and gradient methods used to infer climate change effects on plant communities yield consistent patterns. Proc. Natl Acad. Sci. USA 112, 448–452 (2015).

    CAS  Article  Google Scholar 

  65. 65.

    Hollister, R. D. et al. Warming experiments elucidate the drivers of observed directional changes in tundra vegetation. Ecol. Evol. 5, 1881–1895 (2015).

    Article  Google Scholar 

  66. 66.

    Molau, U. & Mølgaard, P. International Tundra Experiment (ITEX) Manual (Danish Polar Center, 1996).

  67. 67.

    Henry, G. H. R. & Molau, U. Tundra plants and climate change: the International Tundra Experiment (ITEX). Glob. Change Biol. 3, 1–9 (1997).

    Article  Google Scholar 

  68. 68.

    Harris, I., Jones, P, Osborn, T. J. & Lister, D. H. Updated high-resolution grids of monthly climatic observations—the CRU TS3.10 dataset. Int. J. Climatol. 34, 623–642 (2014).

    Article  Google Scholar 

  69. 69.

    Marion, G. M. et al. Open-top designs for manipulating field temperature in high-latitude ecosystems. Glob. Change Biol. 3, 20–32 (1997).

    Article  Google Scholar 

  70. 70.

    Hollister, R. D., Webber, P. J., Nelson, F. E. & Tweedie, C. E. Soil thaw and temperature response to air warming varies by plant community: results from an open-top chamber experiment in Northern Alaska. Arct. Antarct. Alp. Res. 38, 206–215 (2006).

    Article  Google Scholar 

  71. 71.

    Walker, M. D. et al. Plant community responses to experimental warming across the tundra biome. Proc. Natl Acad. Sci. USA 103, 1342–1346 (2006).

    CAS  Article  Google Scholar 

  72. 72.

    Latimer, A. M. Geography and resource limitation complicate metabolism-based predictions of species richness. Ecology 88, 1895–1898 (2007).

    Article  Google Scholar 

  73. 73.

    Stan Modeling Language User’s Guide and Reference Manual Version 2.17.0 (Stan Development Team, 2017).

  74. 74.

    RStan: the R Interface to Stan R Package Version 2.17.3 (Stan Development Team, 2018).

  75. 75.

    R Development Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2017).

  76. 76.

    Gelman, A. & Rubin, D. B. Inference from iterative simulation using multiple sequences. Stat. Sci. 7, 457–472 (1992).

    Article  Google Scholar 

  77. 77.

    Miller-Rushing, A. J., Inouye, D. W. & Primack, R. B. How well do first flowering dates measure plant responses to climate change? The effects of population size and sampling frequency. J. Ecol. 96, 1289–1296 (2008).

    Article  Google Scholar 

Download references


We are grateful to the many individuals who established experiments and collected detailed phenological observations. There are too many to name them all; however, we especially thank: M. Dalle Fratte, D. Cooley, O. Durey, C. Eckert, J. F. Johnstone, C. Kennedy, V. Lamarre, G. Levasseur, C. Spiech, J. Svoboda and R. Wising; the Herschel Island Qikiqtaruk Territorial Park staff, including E. McLeod, S. McLeod, R. Joe, P. Lennie, D. Arey, L. Meyook, J. McLeod, P. Foisy, C. Gordon, J. Hansen, A. Rufus and R. Gordon; Quttinirpaaq National Park staff; the Greenland Ecosystem Monitoring team; and Warming and species Removal in Mountains (WaRM) coordinators N. Sanders, A. Classen and M. Sundqvist. These observations were made possible with the support of many funding agencies and grants, including: ArcticNet; the Natural Sciences and Engineering Research Council of Canada; the Canadian International Polar Year Program; the Polar Continental Shelf Program of Natural Resources Canada; the Danish Environmental Protection Agency; the Swiss Federal Institute for Forest, Snow and Landscape Research; the National Geographic Society; the US National Science Foundation (grant numbers PLR1525636, PLR1504141, PLR1433063, PLR1107381, PLR0119279, PLR0902125, PLR0856728, PLR1312402, PLR1019324, LTER 1026415, OPP1525636, OPP9907185, DEB1637686, 0856710, 9714103, 0632263, 0856516, 1432277, 1432982, 1504381, 1504224, 1433063, 0856728, 0612534, 0119279 and 9421755; the Danish National Research Foundation (grant CENPERM DNRF100); the Danish Council for Independent Research (Natural Sciences grant DFF 4181-00565); the Deutsche Forschungsgemeinschaft (grant: RU 1536/3-1); the Natural Environment Research Council (grant NE/M016323/1); the Department of Energy (grant SC006982); a Semper Ardens grant from the Carlsberg Foundation to N. J. Sanders; and an INTERACT Transnational Access grant. This work was supported by the Norwegian Research Council SnoEco project, grant number 230970.

Author information




J.S.P. and C.R. designed and led the study. J.S.P. and C.R. led the collection of data for the phenology database. J.S.P., N.R., A.D.B., I.H.M.-S. and S.C.E. performed the statistical analyses. J.S.P., C.R., N.R., T.T.H., A.D.B., I.H.M.-S. and S.C.E. drafted the paper. J.S.P., C.R., A.D.B., I.H.M.-S., I.W.A., N.C., K.C., C.C., E.J.C., B.E., A.M.F., G.H.R.H., R.D.H., I.S.J., K.K., C.W.K., E.L., M.M., U.M., S.N., S.O., Z.A.P., E.P., S.B.R., N.M.S., E.S., P.R.S., J.G.S., K.N.S., Ø.T., T.T., S.V., C.-H.W., J.M.W. and S.W. contributed data. All authors were involved in writing and editing the manuscript.

Corresponding author

Correspondence to Janet S. Prevéy.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Tables 1–7, Supplementary Figure 1, Supplementary Code and Supplementary References

Reporting Summary

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Prevéy, J.S., Rixen, C., Rüger, N. et al. Warming shortens flowering seasons of tundra plant communities. Nat Ecol Evol 3, 45–52 (2019).

Download citation

Further reading


Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing