International Journal of Biometeorology

, Volume 57, Issue 4, pp 579–588 | Cite as

Recurring weather extremes alter the flowering phenology of two common temperate shrubs

  • L. Nagy
  • J. Kreyling
  • E. Gellesch
  • C. Beierkuhnlein
  • A. Jentsch
Original Paper


The aim of this study is to explore the effects of heavy rain and drought on the flowering phenology of two shrub species Genista tinctoria and Calluna vulgaris. We conducted a field experiment over five consecutive years in Central Europe, applying annually recurring extreme drought and heavy rain events on constructed shrubland communities and recorded the flowering status. Further, we correlated spring temperature and precipitation with the onset of flowering. Both species showed a response to extreme weather events: drought delayed the mid flowering date of Genista tinctoria in 3 of 5 years by about 1 month and in 1 year advanced the mid flowering date by 10 days, but did not affect the length of flowering. Mid flowering date of Calluna vulgaris was not affected by drought, but the length of flowering was extended in 2 years by 6 and 10 days. For C. vulgaris the closer the drought occurred to the time of flowering, the larger the impact on the flowering length. Heavy rainfall advanced mid flowering date and reduced the length of flowering of Genista tinctoria by about 2 months in 1 year. Mid flowering date of Calluna vulgaris was not affected by heavy rain, but the length of flowering was reduced in 1 year by 4 days. Our data suggest that extreme weather events, including alterations to the precipitation regime, induce phenological shifts of plant species of a substantial magnitude. Thus, the impacts of climate extremes on plant life cycles may be as influential as gradual warming. Particularly, the variability in the timing of precipitation events appears to have a greater influence on flowering dynamics than the magnitude of the precipitation.


Flowering Climate change Extreme drought Phenological alteration Dwarf shrub Precipitation change 



This research project was funded by the “Bavarian Climate Programme 2020” at the joint research center “FORKAST” as well as by DFG (JE 282/6–1). We gratefully acknowledge the help of students and field workers in recording flower phenology and maintaining the plots in the EVENT-experiment. We thank the anonymous reviewers as well as David Inouye as a reviewer for their useful comments.


  1. Boggs CL, Inouye DW (2012) A single climate driver has direct and indirect effects on insect population dynamics. Ecol Lett 15:502–508CrossRefGoogle Scholar
  2. Breshears DD, Cobb NS, Rich PM, Price KP, Allen CD, Balice RG, Romme WH, Kastens JH, Floyd ML, Belnap J, Anderson JJ, Myers OB, Meyer CW (2005) Regional vegetation die-off in response to global-change-type drought. PNAS 42:15144–15148CrossRefGoogle Scholar
  3. Chaves MM, Maroco JP, Pereira JS (2003) Understanding plant responses to drought—from genes to the whole plant. Funct Plant Biol 30:239–264CrossRefGoogle Scholar
  4. Cleland EE, Chiariello NR, Loarie SR, Mooney HA, Field CB (2006) Diverse responses of phenology to global changes in a grassland ecosystem. PNAS 103:13740–13744CrossRefGoogle Scholar
  5. 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
  6. Dose V, Menzel A (2006) Bayesian correlation between temperature and blossom onset data. Glob Change Biol 12:1451–1459CrossRefGoogle Scholar
  7. Ellenberg H (1979) Zeigerwerte der Gefäßpflanzen Mitteleuropas. Goltze, GöttingenGoogle Scholar
  8. Estrella N, Sparks TH, Menzel A (2007) Trends and temperature response in the phenology of crops in German. Glob Change Biol 13:1737–1747CrossRefGoogle Scholar
  9. Faraway JJ (2005) Linear Models with R. Chapman & Hall/CRC, Boca RatonGoogle Scholar
  10. Fitter AH, Fitter RSR (2002) Rapid changes in flowering time in British plants. Science 296:1689–1691CrossRefGoogle Scholar
  11. Galen C, Sherry RA, Carroll AB (1999) Are flowers physiological sinks or faucets? Costs and correlates of water use by flowers of Polemonium viscosum. Oecologia 118:461–470CrossRefGoogle Scholar
  12. Gordon C, Woodin SJ, Alexander IJ, Mullins CE (1999a) a) Effects of increased temperature, drought and nitrogen supply on two upland perennials of contrasting functional type: Calluna vulgaris and Pteridium aquilinum. New Phytol 42:243–258CrossRefGoogle Scholar
  13. Gordon C, Woodin SJ, Mullins CE, Alexander IJ (1999b) Effects of environmental change, including drought, on water use by competing Calluna vulgaris (heather) and Pteridium aquilinium (bracken). Funct Ecol 13:96–106CrossRefGoogle Scholar
  14. Gumbel EJ (1958) Statistics of extremes. Columbia University Press, New YorkGoogle Scholar
  15. Harrison RD (2000) Repercussions of El Nino: drought causes extinction and breakdown of mutualism in Borneo. Proc R Soc B 267:911–915CrossRefGoogle Scholar
  16. IPCC (2007) Climate change 2007: the physical science basis. Contribution to working group I to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, CambridgeGoogle Scholar
  17. Jentsch A, Beierkuhnlein C (2008) Research frontiers in climate change: Effects of extreme meteorological events on ecosystems. CR Geosci 340:621–628CrossRefGoogle Scholar
  18. Jentsch A, Beierkuhnlein C (2010) Simulating the future—responses of ecosystems, key species and European provenances to expected climatic trends and events. Nova Acta Leopoldina 112:89–98Google Scholar
  19. Jentsch A, Kreyling J, Beierkuhnlein C (2007) A new generation of climate-change experiments: events, not trends. Front Ecol Environ 7:365–374CrossRefGoogle Scholar
  20. Jentsch A, Kreyling J, Boettcher-Treschkow J, Beierkuhnlein C (2009) Beyond gradual warming: extreme weather events alter flower phenology of European grassland and heath species. Glob Change Biol 15:837–849CrossRefGoogle Scholar
  21. Kehl M, Everding C, Botschek J, Skowronek A (2005) Erosion processes and erodibility of cultivated soils in North Rhine-Westphalia under artificial rain—I, Site characteristics and results of laboratory experiments. J Plant Nutr Soil Sc 168:34–44CrossRefGoogle Scholar
  22. Llorens L, Penuelas J (2005) Experimental evidence of future drier and warmer conditions affecting flowering of two co-occurring Mediterranean shrubs. Int J Plant Sci 166:235–245CrossRefGoogle Scholar
  23. McDonald AJ, Davies WJ (1996) Keeping in touch: Responses of the whole plant to deficits in water and nitrogen supply. Adv Bot Res 22:229–300CrossRefGoogle Scholar
  24. McKinney AM, CaraDonna PJ, Inouye DW, Barr WA, Bertelsen CD, Waser NM (2012) Asynchronous changes in phenology of migrating Broad-tailed Hummingbirds and their early-season nectar resources. Ecology (in press) Accessed 11 August 2012
  25. Melian CJ, Bascompte J (2002) Complex networks: two ways to be robust? Ecol Lett 5:705–708CrossRefGoogle Scholar
  26. Memmott J, Waser NM, Price MV (2004) Tolerance of pollination networks to species extinctions. P Roy Soc B-Biol Sci 271:2605–2611CrossRefGoogle Scholar
  27. Memmott J, Craze PG, Waser NM, Price MV (2007) Global warming and the disruption of plant-pollinator interactions. Ecol Lett 10:710–717CrossRefGoogle Scholar
  28. Menzel A (2000) Trends in phenological phases in Europe between 1951 and 1996. Int J Biometeorol 44:76–81CrossRefGoogle Scholar
  29. Menzel A, Fabian P (1999) Growing season extended in Europe. Nature 397:659CrossRefGoogle Scholar
  30. Menzel A, Jakobi G, Ahas R, Scheifinger H, Estrella N (2003) Variations of the climatological growing season (1951–2000) in Germany compared with other countries. Int J Climatol 23:793–812CrossRefGoogle Scholar
  31. Menzel A, Sparks TH, Estrella N, Koch E, Aasa A, Ahas R, Alm-Kuebler K, Bissolli P, Braslavska O, Briede A, Chmielewski FM, Crepinsek Z, Curnel Y, Dahl A, Defila C, Donnelly A, Filella Y, Jatcza K, Mage F, Mestre A, Nordli O, Penuelas J, Pirinen P, Remisova V, Scheifinger H, Striz M, Susnik A, van Vliet AJH, Wielgolaski F, Zach S, Zust A (2006) European phenological response to climate change matches the warming pattern. Glob Change Biol 12:1969–1976CrossRefGoogle Scholar
  32. Murphy DD, Launer AE, Ehrlicher PR (1983) The role of adult feeding in egg production and population dynamics of the checkerspot butterfly Euphydryas editha. Ecologia 56:257–263Google Scholar
  33. O’Gorman PA, Schneider T (2009) The physical basis for increases in precipitation extremes in simulations of 21st-century climate change. PNAS 106:14773–14777CrossRefGoogle Scholar
  34. Ollerton J, Lack A (1998) Relationships between flowering phenology, plant size and reproductive success in Lotus corniculatus (Fabaceae). Plant Ecol 139:35–47CrossRefGoogle Scholar
  35. Parmesan C (2007) Influences of species, latitudes and methodologies on estimates of phenological response to global warming. Glob Change Biol 13:1860–1872CrossRefGoogle Scholar
  36. Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42CrossRefGoogle Scholar
  37. Parmesan C, Root TL, Willig MR (2000) Impacts of extreme weather and climate on terrestrial biota. Bull Amer Meteor Soc 81:443–450CrossRefGoogle Scholar
  38. Penuelas J, Filella I (2001) Phenology—Responses to a warming world. Science 294:793CrossRefGoogle Scholar
  39. Ploschuk EL, Windauer L, Ravetta DA (2001) Potential value of traits associated with perennial habit in the development of new oil-seed crops for arid lands, A comparison of Lesquerella fendleri and L, mendocina subjected to water stress. J Arid Environ 47:373–386CrossRefGoogle Scholar
  40. Prieto P, Penuelas J, Ogaya R, Estiarte M (2008) Precipitation-dependent flowering of Globularia alypum and Erica multiflora in Mediterranean shrubland under experimental drought and warming, and its inter-annual variability. Ann Bot 102:275–285CrossRefGoogle Scholar
  41. Prieto P, Penuelas J, Niinemets U, Ogaya R, Schmidt IK, Beier C, Tietema A, Sowerby A, Emmett BA, Lang EK, Kroel-Dulay G, Lhotsky B, Cesaraccio C, Pellizzaro G, de Dato G, Sirca C, Estiarte M (2009) Changes in the onset of spring growth in shrubland species in response to experimental warming along a north–south gradient in Europe. Global Ecol Biogeogr 18:473–484CrossRefGoogle Scholar
  42. R Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN: 3-900051-07-0. URL: Accessed 11 August 2012
  43. Rodrigues ML, Pacheco CM, Chaves MM (1995) Soil—plant water relations, root distribution and partitioning in Lupinus-Albus L under drought. J Exp Bot 46:947–956CrossRefGoogle Scholar
  44. Royer PD, Cobb NS, Clifford MJ, Huang C, Breshears DD, Adams HD, Camilo VJ (2011) Extreme climatic events-triggered overstorey vegetation loss increases understory solar input regionally: primary and secondary ecological implication. J Ecol 3:714–723CrossRefGoogle Scholar
  45. Schleip C, Sparks TH, Estrella N, Menzel A (2009) Spatial variation in onset dates and trends in phenology across Europe. Clim Res 39:249–260CrossRefGoogle Scholar
  46. Sharp RE, LeNoble ME (2002) ABA, ethylene and the control of shoot and root growth under water stress. J Exp Bot 53:33–37CrossRefGoogle Scholar
  47. Sherry RA, Zhou X, Gu S, Arnone IJA, Schimel DS, Verburg PS, Wallace LL, Luo Y (2007) Divergence of reproductive phenology under climate warming. P Natl Acad USA 104:198–202CrossRefGoogle Scholar
  48. Sherry RA, Zhou X, Gu S, Shiliang G, Arnone JA, Johnsosn DW, Schimel DS, Verburg PS, Wallace LL, Luo Y (2011) Changes in duration of reproductive phases and lagged phenological response to experimental climate warming. Plant Ecol Div 4:23–35CrossRefGoogle Scholar
  49. Sparks TH, Menzel A (2002) Observed changes in seasons: An overview. Int J Climatol 22:1715–1725CrossRefGoogle Scholar
  50. Sparks TH, Menzel A, Stenseth NC (2009) European cooperation in plant phenology. Clim Res 39:175–177CrossRefGoogle Scholar
  51. Thomson JD (2010) Flowering phenology, fruiting success and progressive deterioration of pollination in an early-flowering geophyte. Philos Trans R Soc Lond B Biol Sci 365:3187–3199CrossRefGoogle Scholar
  52. Toh S, Imamura A, Watanabe A, Nakabayashi K, Okamoto M, Jikumaru Y, Hanada A, Aso Y, Ishiyama K, Tamura N, Iuchi S, Kobayashi M, Yamaguchi S, Kamiya Y, Nambara E, Kawakami N (2008) High temperature-induced abscisic acid biosynthesis and its role in the inhibition of gibberellin action in Arabidopsis seeds. Plant Physiol 146:1368–1385CrossRefGoogle Scholar
  53. Wall MA, Timmerman-Erskine M, Boyd RS (2003) Conservation impact of climatic variability on pollination of the federally endangered plant, Clematis socialis (Ranunculaceae). Southeast Nat 2:11–24CrossRefGoogle Scholar
  54. Walther GR, Post E, Convey P, Menzel A, Parmesan C, Beebee TJ, Fromentin JM, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416:389–395CrossRefGoogle Scholar
  55. Wielgolaski FE (2001) Phenological modifications in plants by various edaphic factors. Int J Biometeorol 45:196–202CrossRefGoogle Scholar
  56. Zavaleta ES, Shaw CNR, Thomas BD, Cleland EE, Field CB, Mooney HA (2003) Grassland responses to three years of elevated temperature, CO2, precipitation, and N deposition. Ecol Monogr 73:585–604CrossRefGoogle Scholar

Copyright information

© ISB 2012

Authors and Affiliations

  • L. Nagy
    • 1
  • J. Kreyling
    • 2
  • E. Gellesch
    • 1
  • C. Beierkuhnlein
    • 2
  • A. Jentsch
    • 1
  1. 1.Disturbance EcologyUniversity of BayreuthBayreuthGermany
  2. 2.BiogeographyUniversity of BayreuthBayreuthGermany

Personalised recommendations