International Journal of Biometeorology

, Volume 60, Issue 10, pp 1551–1561 | Cite as

Can we detect a nonlinear response to temperature in European plant phenology?

  • Susanne JochnerEmail author
  • Tim H. Sparks
  • Julia Laube
  • Annette Menzel
Original Paper


Over a large temperature range, the statistical association between spring phenology and temperature is often regarded and treated as a linear function. There are suggestions that a sigmoidal relationship with definite upper and lower limits to leaf unfolding and flowering onset dates might be more realistic. We utilised European plant phenological records provided by the European phenology database PEP725 and gridded monthly mean temperature data for 1951–2012 calculated from the ENSEMBLES data set E-OBS (version 7.0). We analysed 568,456 observations of ten spring flowering or leafing phenophases derived from 3657 stations in 22 European countries in order to detect possible nonlinear responses to temperature. Linear response rates averaged for all stations ranged between −7.7 (flowering of hazel) and −2.7 days °C−1 (leaf unfolding of beech and oak). A lower sensitivity at the cooler end of the temperature range was detected for most phenophases. However, a similar lower sensitivity at the warmer end was not that evident. For only ∼14 % of the station time series (where a comparison between linear and nonlinear model was possible), nonlinear models described the relationship significantly better than linear models. Although in most cases simple linear models might be still sufficient to predict future changes, this linear relationship between phenology and temperature might not be appropriate when incorporating phenological data of very cold (and possibly very warm) environments. For these cases, extrapolations on the basis of linear models would introduce uncertainty in expected ecosystem changes.


Climate change Europe Nonlinearity PEP725 Phenology Sigmoid Temperature response 



We thank the PEP725 for their phenological data and the many thousands of people whose observations are summarised there. We acknowledge the E-OBS data set from the EU-FP6 project ENSEMBLES ( and the data providers in the ECA&D project ( The authors gratefully acknowledge the support by the Technische Universität München–Institute for Advanced Study (IAS), funded by the German Excellence Initiative. The research leading to these results has received funding from the European Research Council under the European Union’s Seventh Framework Programme (FP7/2007-2013)/ERC grant agreement no. 282250.

Supplementary material

484_2016_1146_MOESM1_ESM.docx (34 kb)
ESM 1 (DOCX 33 kb)


  1. Barnosky AS, Matzke N, Tomiya S, Wogan GOU, Swartz B, Quental TB, Marshall C, McGuire JL, Lindsey EL, Maguire KC, Mersey B, Ferrer EA (2011) Has the Earth’s sixth mass extinction already arrived? Nature 471(7336):51–57CrossRefGoogle Scholar
  2. Bennie J, Kubin E, Wiltshire A, Huntley B, Baxter R (2010) Predicting spatial and temporal patterns of bud-burst and spring frost risk in north-west Europe: the implications of local adaption to climate. Glob Chang Biol 16:1503–1514CrossRefGoogle Scholar
  3. Caffarra A, Donnelly A, Chuine I (2011a) Modelling the timing of Betula pubescens budburst. II. Integrating complex effects of photoperiod into process-based models. Clim Res 46:159–170CrossRefGoogle Scholar
  4. Caffarra A, Donnelly A, Chuine I, Jones MB (2011b) Modelling the timing of Betula pubescens budburst. I. Temperature and photoperiod: a conceptual model. Clim Res 46:147–157CrossRefGoogle Scholar
  5. Chen I-C, Hill JK, Ohlemüller R, Roy DB, Thomas CD (2011) Rapid range shifts of species associated with high levels of climate warming. Science 333(6045):1024–1026CrossRefGoogle Scholar
  6. Cleland EE, Chuine I, Menzel A, Mooney HA, Schwartz MD (2007) Shifting plant phenology in response to global change. Trends Ecol Evol 22:357–365CrossRefGoogle Scholar
  7. Cook BI, Wolkovich EM, Parmesan C (2012) Divergent responses to spring and winter warming drive community level flowering trends. PNAS 109:9000–9005CrossRefGoogle Scholar
  8. Dantec CF, Vitasse Y, Bonhomme M, Louvet J-M, Kremer A, Delzon S (2014) Chilling and heat requirements for leaf unfolding in European beech and sessile oak populations at the southern limit of their distribution range. Int J Biometeorol 58(9):1853–1864CrossRefGoogle Scholar
  9. de Réaumur RAF (1735) Observations du thermomètre, faites à Paris pendant l’annee 1735, comparées avec celles qui ont été faites sous la ligne, á l’isle de France, á Alger et quelques unes des nos isles de l’Amérique. Mem Acad des Sci, Paris: 545Google Scholar
  10. Defila C, Clot B (2001) Phytophenological trends in Switzerland. Int J Biometeorol 45:203–207CrossRefGoogle Scholar
  11. Delbart N, Le Toan T, Kergoat L, Fedotova V (2006) Remote sensing of spring phenology in boreal regions: a free of snow-effect method using NOAA-AVHRR and SPOT-VGT data (1982–2004). Remote Sens Environ 101(1):52–62CrossRefGoogle Scholar
  12. Dose V, Menzel A (2006) Bayesian correlation between temperature and blossom onset data. Glob Chang Biol 12(9):1451–1459CrossRefGoogle Scholar
  13. Ellwood ER, Temple SA, Primack RB, Bradley NL, Davis CC (2013) Record-breaking early flowering in the Eastern United States. PLoS One 8(1):e53788. doi: 10.1371/journal.pone.0053788 CrossRefGoogle Scholar
  14. Estrella N, Sparks TH, Menzel A (2007) Trends and temperature response in the phenology of crops in Germany. Glob Change Biol 13:1737–1747CrossRefGoogle Scholar
  15. European Environment Agency (EEA) (2010) CORINE Land Cover (CLC) 2006 raster data 100 × 100 m—version 13 (02/2010). Available at
  16. Fu YH, Zhao H, Piao S, Peaucelle M, Peng S, Zhou G, Ciais P, Huang M, Menzel A, Peñuelas J, Song Y, Vitasse Y, Zeng Z, Janssens IA (2015) Declining global warming effects on the phenology of spring leaf unfolding. Nature 526:104–107CrossRefGoogle Scholar
  17. Gazal R, White MA, Gillies R, Rodemaker E, Sparrow E, Gordon L (2008) GLOBE students, teachers, and scientists demonstrate variable differences between urban and rural leaf phenology. Glob Chang Biol 14:1568–1580CrossRefGoogle Scholar
  18. Hänninen H, Kellomäki S, Laitinen K, Pajari B, Repo T (1993) Effect of increased winter temperature on the onset of height growth of Scots pine: a field test of a phenological model. Silva Fennica 27:251–257CrossRefGoogle Scholar
  19. Haylock MR, Hofstra N, Klein Tank AMG, Klok EJ, Jones PD, New M (2008) A European daily high-resolution gridded dataset of surface temperature and precipitation. J Geophys Res Atmos 113:D20119. doi: 10.1029/2008JD10201 CrossRefGoogle Scholar
  20. Heide OM (2003) High autumn temperature delays spring bud burst in boreal trees, counterbalancing the effect of climatic warming. Tree Physiol 23:931–936CrossRefGoogle Scholar
  21. Hill JK, Thomas CD, Blakeley DS (1999) Evolution of flight morphology in a butterfly that has recently expanded its geographic range. Oecologia 121(2):165–170CrossRefGoogle Scholar
  22. Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6:65–70Google Scholar
  23. IPCC (2013) Summary for policymakers. In: Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Eds. Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM, Cambridge University PressGoogle Scholar
  24. Jochner S, Sparks TH, Estrella N, Menzel A (2012) The influence of altitude and urbanisation on trends and mean dates in phenology (1980-2009). Int J Biometeorol 56:387–394CrossRefGoogle Scholar
  25. Körner C (2004) Mountain biodiversity, its causes and functions. Ambio Special Report 13:11–17Google Scholar
  26. Körner C, Basler D (2010) Phenology under global warming. Science 327:1461–1462CrossRefGoogle Scholar
  27. Landsberg HE (1981) The urban climate. Academic PressGoogle Scholar
  28. Lapenis A, Henry H, Vuille M, Mower J (2014) Climatic factors controlling plant sensitivity to warming. Clim Change 122:723–734CrossRefGoogle Scholar
  29. Laube J, Sparks TH, Estrella N, Höfler J, Ankerst DP, Menzel A (2014) Chilling outweighs photoperiod in preventing precocious spring development. Glob Change Biol 20(1):170–182CrossRefGoogle Scholar
  30. Lenoir J, Svenning J-C (2014) Climate-related range shifts—a global multidimensional synthesis and new research directions. Ecography. doi: 10.1111/ecog.00967 Google Scholar
  31. Lu P, Yu Q, Liu J, Lee X (2006) Advance of tree-flowering dates in response to urban climate change. Agri For Meteorol 138:120–131CrossRefGoogle Scholar
  32. Luo Z, Sun OJ, Ge Q, Xu W, Zheng J (2007) Phenological responses of plants to climate change in an urban environment. Ecol Res 22:507–514CrossRefGoogle Scholar
  33. Luyssaert S, Ciais P, Piao SL, Schulze E-D, Jung M, Zaehle S, Schelhaas MJ, Reichstein M, et al. (2010) The European carbon balance. Part 3: forests. Glob Change Biol 16(5):1429–1450CrossRefGoogle Scholar
  34. Meier U (Ed.) (2001) Entwicklungsstadien mono- und dikotyler Pflanzen. BBCH-Monograph. Biologische Bundesanstalt für Land und ForstwirtschaftGoogle Scholar
  35. Menzel A, Estrella N, Testka A (2005) Temperature response rates from long-term phenological records. Clim Res 30:21–28CrossRefGoogle Scholar
  36. Menzel A, Sparks TH, Estrella N, Koch E, Aasa A, Ahas R, Alm-Kübler K, Bissoli P, et al. (2006) European phenological response to climate change matches the warming pattern. Glob Chang Biol 12:1969–1976CrossRefGoogle Scholar
  37. Morin X, Lechowicz MJ, Augspurger C, O’ Keefe J, Viner D, Chuine I (2009) Leaf phenology in 22 North American tree species during the 21st century. Glob Change Biol 15:961–975CrossRefGoogle Scholar
  38. Morin X, Roy J, Sonié L, Chuine I (2010) Changes in leaf phenology of three European oak species in response to experimental climate change. New Phytol 186:900–910CrossRefGoogle Scholar
  39. Murray MB, Cannell MGR, Smith RI (1989) Date of budburst of fifteen tree species in Britain following climatic warming. J Appl Ecol 26(2):693–700CrossRefGoogle Scholar
  40. Newnham RM, Sparks TH, Skjøth CA, Head K, Adams-Groom B, Smith M (2013) Pollen season and climate: Is the timing of birch pollen release in the UK approaching its limit? Int J Biometeorol 57:391–400CrossRefGoogle Scholar
  41. Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42CrossRefGoogle Scholar
  42. Partanen J, Koski V, Hänninen H (1998) Effects of photoperiod and temperature on the timing of bud burst in Norway spruce (Picea abies). Tree Physiol 18:811–816CrossRefGoogle Scholar
  43. Polgar C, Gallinat A, Primack RB (2014) Drivers of leaf-out phenology and their implications for species invasions: insights from Thoreau’s concord. New Phytol 202(1):106–115CrossRefGoogle Scholar
  44. Pope KS, Dose V, Da Silva D, Brown PH, Leslie CA, Dejong TM (2013) Detecting nonlinear response of spring phenology to climate change by Bayesian analysis. Glob Chang Biol 19(5):1518–1555CrossRefGoogle Scholar
  45. Primack RB, Ibáñez I, Higuchi H, Lee SD, Miller-Rushing AJ, Wilson AM, Silander JA (2009) Spatial and interspecific variability in phenological responses to warming temperatures. Biol Conserv 142:2569–2577CrossRefGoogle Scholar
  46. Root TL, Price JT, Hall KR, Schneider SH, Rosenzweig C, Pounds AJ (2003) Fingerprints of global warming on wild animals and plants. Nature 421:57–60CrossRefGoogle Scholar
  47. Rosenzweig C, Karoly D, Vicarelli M, Neofotis P, Wu Q, Casassa G, Menzel A, Root TL, Estrella N, Seguin B, Tryjanowski P, Liu C, Rawlins S, Imeson A (2008) Attributing physical and biological impacts to anthropogenic climate change. Nature 453:353–357CrossRefGoogle Scholar
  48. Schwartz MD (1997) Spring index models: an approach to connecting satellite and surface phenology. In: Phenology of Seasonal Climates. Eds. Lieth H, Schwartz MD. Backhuys: 23–38Google Scholar
  49. Shen M (2011) Spring phenology was not consistently related to winter warming on the Tibetan Plateau. PNAS 108(19):E91–E92CrossRefGoogle Scholar
  50. Sparks TH, Jeffree EP, Jeffree CE (2000) An examination of the relationship between flowering times and temperature at the national scale using long-term phenological records from the UK. Int J Biometeorol 44:82–87CrossRefGoogle Scholar
  51. Sparks TH, Menzel A, Peñuelas J, Tryjanowski P (2011) Species response to contemporary climate change. Millington AC, Blumler M, Schickhoff U (eds.), The SAGE handbook of biogeography. SAGE, pp. 231–242Google Scholar
  52. Tryjanowski P, Panek M, Sparks T (2006) Phenological response of plants to temperature varies at the same latitude: case study of dog violet and horse chestnut in England and Poland. Clim Res 32:89–93CrossRefGoogle Scholar
  53. Vitasse Y, Delzon S, Bresson CC, Michalet R, Kremer A (2009) Altitudinal differentiation in growth and phenology among populations of temperate-zone tree species growing in a common garden. Can J For Res 39:1259–1269CrossRefGoogle Scholar
  54. Vitasse Y, Hoch G, Randin CF, Lenz A, Kollas C, Scheepens JF, Körner C (2013) Elevational adaptations and plasticity in seedling phenology of temperate deciduous tree species. Oecologia 171:663–678CrossRefGoogle Scholar
  55. Walther G-R (2000) Climatic forcing on the dispersal of exotic species. Phytocoenologia 30(3–4):409–430Google Scholar
  56. Walther G-R, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC, Frometin J-M, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416:389–395CrossRefGoogle Scholar
  57. Wang SP, Meng FD, Duan JC, Wang YF, Cui XY, Piao L, Niu HS, Xu GP, et al. (2014) Asymmetric sensitivity of first flowering date to warming and cooling in alpine plants. Ecology 95(12):3387–3398CrossRefGoogle Scholar
  58. Wolkovich EM, Cook BI, Allen JM, Crimmins TM, Betancourt JL, Travers SE, Pau S, Regetz J, et al. (2012) Warming experiments underpredict plant phenological responses to climate change. Nature 485:494–497Google Scholar
  59. Yu H, Luedeling E, Xu J (2010) Winter and spring warming result in delayed spring phenology on the Tibetan Plateau. PNAS 107:22151–22156CrossRefGoogle Scholar
  60. Zhang XY, Tarpley D, Sullivan JT (2007) Diverse responses of vegetation phenology to a warming climate. Geophys Res Lett 34:1–5Google Scholar
  61. Ziello C, Sparks TH, Estrella N, Belmonte J, Bergmann KC, Bucher E, Brighetti MA, Damialis A, et al. (2012) Changes to airborne pollen counts across Europe. PLoS One 7:e34076CrossRefGoogle Scholar

Copyright information

© ISB 2016

Authors and Affiliations

  • Susanne Jochner
    • 1
    • 2
    • 3
    Email author
  • Tim H. Sparks
    • 2
    • 3
    • 4
    • 5
  • Julia Laube
    • 2
    • 3
  • Annette Menzel
    • 2
    • 3
  1. 1.Physical Geography/Landscape Ecology and Sustainable Ecosystem DevelopmentCatholic University Eichstätt-IngolstadtEichstättGermany
  2. 2.Department of Ecology and Ecosystem Management, EcoclimatologyTechnische Universität MünchenFreisingGermany
  3. 3.Institute for Advanced StudyTechnische Universität MünchenGarchingGermany
  4. 4.Institute of ZoologyPoznań University of Life SciencesPoznańPoland
  5. 5.Sigma/Faculty of Engineering, Environment and ComputingCoventry UniversityCoventryUK

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