Advertisement

International Journal of Biometeorology

, Volume 61, Issue 2, pp 349–361 | Cite as

‘Hearing’ alpine plants growing after snowmelt: ultrasonic snow sensors provide long-term series of alpine plant phenology

  • Yann VitasseEmail author
  • Martine Rebetez
  • Gianluca Filippa
  • Edoardo Cremonese
  • Geoffrey Klein
  • Christian Rixen
Original Paper

Abstract

In alpine environments, the growing season is severely constrained by low temperature and snow. Here, we aim at determining the climatic factors that best explain the interannual variation in spring growth onset of alpine plants, and at examining whether photoperiod might limit their phenological response during exceptionally warm springs and early snowmelts. We analysed 17 years of data (1998–2014) from 35 automatic weather stations located in subalpine and alpine zones ranging from 1560 to 2450 m asl in the Swiss Alps. These stations are equipped with ultrasonic sensors for snow depth measurements that are also able to detect plant growth in spring and summer, giving a unique opportunity to analyse snow and climate effects on alpine plant phenology. Our analysis showed high phenological variation among years, with one exceptionally early and late spring, namely 2011 and 2013. Overall, the timing of snowmelt and the beginning of plant growth were tightly linked irrespective of the elevation of the station. Snowmelt date was the best predictor of plant growth onset with air temperature after snowmelt modulating the plants’ development rate. This multiple series of alpine plant phenology suggests that currently alpine plants are directly tracking climate change with no major photoperiod limitation.

Keywords

Phenology Snowmelt Alpine vegetation Climate warming Growth onset Photoperiod Thermal time Ultrasonic sensor 

Notes

Acknowledgments

We are grateful to Marcel Schoch and Christoph Marty for their assistance in providing climate parameters from the IMIS weather stations and to Andreas Scharl and André Fichtner for their field assistance with the vegetation surveys at the weather stations. We thank Andreas Stoffel for drawing the map of the selected stations shown in Fig. 1. We are grateful to David Inouye for his valuable comments on the manuscript and William Doehler for his editorial improvements of the manuscript. The research leading to these results has been funded by the Swiss National Science Foundation (grant number 200021-152954).

Supplementary material

484_2016_1216_MOESM1_ESM.pdf (47 kb)
Table S1 (PDF 47 kb)
484_2016_1216_MOESM2_ESM.pdf (45 kb)
Table S2 (PDF 45 kb)

References

  1. Anderson JT, Inouye DW, McKinney AM, Colautti RI, Mitchell-Olds T (2012) Phenotypic plasticity and adaptive evolution contribute to advancing flowering phenology in response to climate change. Proceedings of the Royal Society B-Biological Sciences 279:3843–3852CrossRefGoogle Scholar
  2. Basler D (2016) Evaluating phenological models for the prediction of leaf-out dates in six temperate tree species across Central Europe. Agric For Meteorol 217:10–21CrossRefGoogle Scholar
  3. Basler D, Körner C (2012) Photoperiod sensitivity of bud burst in 14 temperate forest tree species. Agric For Meteorol 165:73–81CrossRefGoogle Scholar
  4. Bjorkman AD, Elmendorf SC, Beamish AL, Vellend M, Henry GH (2015) Contrasting effects of warming and increased snowfall on Arctic tundra plant phenology over the past two decades. Glob Chang Biol 21:4651–4661CrossRefGoogle Scholar
  5. Böhm R, Auer I, Brunetti M, Maugeri M, Nanni T, Schöner W (2001) Regional temperature variability in the European Alps: 1760–1998 from homogenized instrumental time series. Int J Climatol 21:1779–1801CrossRefGoogle Scholar
  6. CaraDonna PJ, Inouye DW (2015) Phenological responses to climate change do not exhibit phylogenetic signal in a subalpine plant community. Ecology 96:355–361CrossRefGoogle Scholar
  7. Chen X, An S, Inouye DW, Schwartz MD (2015) Temperature and snowfall trigger alpine vegetation green-up on the world's roof. Glob Chang Biol 21:3635–3646CrossRefGoogle Scholar
  8. Clark JS, Salk C, Melillo J, Mohan J, Anten N (2014) Tree phenology responses to winter chilling, spring warming, at north and south range limits. Funct Ecol 28:1344–1355CrossRefGoogle Scholar
  9. Cornelius C, Leingärtner A, Hoiss B, Krauss J, Steffan-Dewenter I, Menzel A (2013) Phenological response of grassland species to manipulative snowmelt and drought along an altitudinal gradient. J Exp Bot 64:241–251CrossRefGoogle Scholar
  10. Efron B, Tibshirani RJ (1994) An introduction to the bootstrap. CRC press, New York: Chapman & HallGoogle Scholar
  11. Ernakovich JG, Hopping KA, Berdanier AB, Simpson RT, Kachergis EJ, Steltzer H, Wallenstein MD (2014) Predicted responses of arctic and alpine ecosystems to altered seasonality under climate change. Glob Chang Biol 20:3256–3269CrossRefGoogle Scholar
  12. Filippa G, Cremonese E, Galvagno M, Migliavacca M, di Cella UM, Petey M, Siniscalco C (2015) Five years of phenological monitoring in a mountain grassland: inter-annual patterns and evaluation of the sampling protocol. Int J Biometeorol 1–11Google Scholar
  13. Fu YH et al. (2015a) Increased heat requirement for leaf flushing in temperate woody species over 1980-2012: effects of chilling, precipitation and insolation. Glob Chang Biol 21:2687–2697CrossRefGoogle Scholar
  14. Fu YH et al. (2015b) Declining global warming effects on the phenology of spring leaf unfolding. Nature 526:104–107CrossRefGoogle Scholar
  15. Fu YSH et al. (2014) Variation in leaf flushing date influences autumnal senescence and next year’s flushing date in two temperate tree species. Proc Natl Acad Sci 111:7355–7360CrossRefGoogle Scholar
  16. Gallinat AS, Primack RB, Wagner DL (2015) Autumn, the neglected season in climate change research. Trends Ecol Evol 30:169–176CrossRefGoogle Scholar
  17. Galvagno M et al. (2013) Phenology and carbon dioxide source/sink strength of a subalpine grassland in response to an exceptionally short snow season. Environ Res Lett 8:025008CrossRefGoogle Scholar
  18. Gobiet A, Kotlarski S, Beniston M, Heinrich G, Rajczak J, Stoffel M (2014) 21st century climate change in the European Alps—A review. Sci Total Environ 493:1138–1151CrossRefGoogle Scholar
  19. Gottfried M et al. (2012) Continent-wide response of mountain vegetation to climate change. Nat Clim Chang 2:111–115CrossRefGoogle Scholar
  20. Grabherr G, Gottfried M, Pauli H (1994) Climate effects on mountain plants. Nature 369:448–448CrossRefGoogle Scholar
  21. Hernández-Henríquez MA, Déry SJ, Derksen C (2015) Polar amplification and elevation-dependence in trends of Northern Hemisphere snow cover extent, 1971–2014. Environ Res Lett 10:044010CrossRefGoogle Scholar
  22. Hülber K, Winkler M, Grabherr G (2010) Intraseasonal climate and habitat-specific variability controls the flowering phenology of high alpine plant species. Funct Ecol 24:245–252CrossRefGoogle Scholar
  23. Iler AM, Høye 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 368:20120489CrossRefGoogle Scholar
  24. Iler AM, Inouye DW (2013) Effects of climate change on mast-flowering cues in a clonal montane herb, Veratrum tenuipetalum (Melanthiaceae). Am J Bot 100:519–525CrossRefGoogle Scholar
  25. Inouye DW (2000) The ecological and evolutionary significance of frost in the context of climate change. Ecol Lett 3:457–463CrossRefGoogle Scholar
  26. Inouye DW (2008) Effects of climate change on phenology, frost damage, and floral abundance of montane wildflowers. Ecology 89:353–362CrossRefGoogle Scholar
  27. Jonas T, Rixen C, Sturm M, Stoeckli V (2008) How alpine plant growth is linked to snow cover and climate variability. Journal of Geophysical Research: Biogeosciences 113:G03013CrossRefGoogle Scholar
  28. Julitta T et al. (2014) Using digital camera images to analyse snowmelt and phenology of a subalpine grassland. Agric For Meteorol 198–199:116–125CrossRefGoogle Scholar
  29. Keller F, Körner C (2003) The role of photoperiodism in alpine plant development. Arct Antarct Alp Res 35:361–368CrossRefGoogle Scholar
  30. Kimball SL, Bennett BD, Salisbury FB (1973) The growth and development of montane species at near-freezing temperatures. Ecology 168–173Google Scholar
  31. Kollas C, Randin CF, Vitasse Y, Körner C (2014) How accurately can minimum temperatures at the cold limits of tree species be extrapolated from weather station data? Agric For Meteorol 184:257–266CrossRefGoogle Scholar
  32. Körner C (2003) Alpine plant life, 2nd edn. Springer, BerlinCrossRefGoogle Scholar
  33. Laternser M, Schneebeli M (2003) Long-term snow climate trends of the Swiss Alps (1931–99). Int J Climatol 23:733–750CrossRefGoogle Scholar
  34. Laube J, Sparks TH, Estrella N, Höfler J, Ankerst DP, Menzel A (2014) Chilling outweighs photoperiod in preventing precocious spring development. Glob Chang Biol 20:170–182CrossRefGoogle Scholar
  35. Livensperger C, Steltzer H, Darrouzet-Nardi A, Sullivan PF, Wallenstein M, Weintraub MN (2016) Earlier snowmelt and warming lead to earlier but not necessarily more plant growth. AoB Plants 8:plw021Google Scholar
  36. Meehl GA et al. (2007) Global climate projections. In: Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, UK and New York, NY, USAGoogle Scholar
  37. Mountain Research Initiative EDWWG (2015) Elevation-dependent warming in mountain regions of the world. Nature Clim Change 5:424–430CrossRefGoogle Scholar
  38. Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annual Review of Ecology Evolution and Systematics 37:637–669CrossRefGoogle Scholar
  39. Parolo G, Rossi G (2008) Upward migration of vascular plants following a climate warming trend in the Alps. Basic and Applied Ecology 9:100–107CrossRefGoogle Scholar
  40. Pauli H et al. (2012) Recent plant diversity changes on Europe’s mountain summits. Science 336:353–355CrossRefGoogle Scholar
  41. Petraglia A, Tomaselli M, Petit Bon M, Delnevo N, Chiari G, Carbognani M (2014) Responses of flowering phenology of snowbed plants to an experimentally imposed extreme advanced snowmelt. Plant Ecol 215:759–768CrossRefGoogle Scholar
  42. R Core Team (2015) cianR: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
  43. Rebetez M, Reinhard M (2008) Monthly air temperature trends in Switzerland 1901–2000 and 1975–2004. Theor Appl Climatol 91:27–34CrossRefGoogle Scholar
  44. Reid PC et al. (2016) Global impacts of the 1980s regime shift. Glob Chang Biol 22:682–703CrossRefGoogle Scholar
  45. Scheepens JF, Stöcklin J (2013) Flowering phenology and reproductive fitness along a mountain slope: maladaptive responses to transplantation to a warmer climate in Campanula thyrsoides. Oecologia 171:679–691CrossRefGoogle Scholar
  46. Scherrer D, Körner C (2010) Infra-red thermometry of alpine landscapes challenges climatic warming projections. Glob Chang Biol 16:2602–2613Google Scholar
  47. Scherrer SC, Appenzeller C (2006) Swiss Alpine snow pack variability: major patterns and links to local climate and large-scale flow. Clim Res 32:187–199CrossRefGoogle Scholar
  48. Sedlacek J et al. (2016) Evolutionary potential in the Alpine: trait heritabilities and performance variation of the dwarf willow Salix herbacea from different elevations and microhabitats. Ecol Evol:in pressGoogle Scholar
  49. Sedlacek J et al. (2015) The response of the alpine dwarf shrub Salix herbacea to altered snowmelt timing: lessons from a multi-site transplant experiment. PLoS One 10:e0122395CrossRefGoogle Scholar
  50. Serquet G, Marty C, Dulex JP, Rebetez M (2011) Seasonal trends and temperature dependence of the snowfall/precipitation-day ratio in Switzerland. Geophys Res Lett 38Google Scholar
  51. Serquet G, Marty C, Rebetez M (2013) Monthly trends and the corresponding altitudinal shift in the snowfall/precipitation day ratio. Theor Appl Climatol 114:437–444CrossRefGoogle Scholar
  52. Wahren CHA, Walker MD, Bret-Harte MS (2005) Vegetation responses in Alaskan arctic tundra after 8 years of a summer warming and winter snow manipulation experiment. Glob Chang Biol 11:537–552CrossRefGoogle Scholar
  53. Walker DA, Halfpenny JC, Walker MD, Wessman CA (1993) Long-term studies of snow-vegetation interactions. Bioscience 43:287–301CrossRefGoogle Scholar
  54. Walther G-R (2003) Plants in a warmer world. Perspectives in plant ecology, evolution and systematics 6:169–185CrossRefGoogle Scholar
  55. Wheeler JA et al. (2016) The snow and the willows: earlier spring snowmelt reduces performance in the low-lying alpine shrub Salix herbacea. J Ecol:in pressGoogle Scholar
  56. Wheeler JA, Hoch G, Cortés AJ, Sedlacek J, Wipf S, Rixen C (2014) Increased spring freezing vulnerability for alpine shrubs under early snowmelt. Oecologia 175:219–229CrossRefGoogle Scholar
  57. Wielgolaski FE, Inouye DW (2013) Phenology at high latitudes. In: Schwartz MD (ed) Phenology: an integrative environmental science. Springer, pp 225–247Google Scholar
  58. Wipf S, Rixen C (2010) A review of snow manipulation experiments in Arctic and alpine tundra ecosystems. Polar Res 29:95–109CrossRefGoogle Scholar
  59. Wipf S, Stoeckli V, Bebi P (2009) Winter climate change in alpine tundra: plant responses to changes in snow depth and snowmelt timing. Clim Chang 94:105–121CrossRefGoogle Scholar
  60. Zohner CM, Renner SS (2015) Perception of photoperiod in individual buds of mature trees regulates leaf-out. New Phytol 208:1023–1030CrossRefGoogle Scholar

Copyright information

© ISB 2016

Authors and Affiliations

  1. 1.Institute of GeographyUniversity of NeuchatelNeuchatelSwitzerland
  2. 2.WSL Swiss Federal Institute for Forest, Snow and Landscape ResearchNeuchatelSwitzerland
  3. 3.WSL Institute for Snow and Avalanche Research SLF, Group Mountain EcosystemsDavosSwitzerland
  4. 4.Environmental Protection Agency of Aosta Valley, ARPA VdA, Climate Change UnitAostaItaly

Personalised recommendations