Abstract
Shifts in flowering phenology of plants are indicators of climate change. The great majority of existing phenological studies refer solely to gradual warming. However, knowledge on how flowering phenology responds to changes in seasonal variation of warming and precipitation regimes is missing. We report the onset of 22 early (flowering before/within May) and 23 late flowering (flowering after May) species in response to manipulated seasonal warming (equal to + 1.2°C; last 100-year summer/winter warming), additional winter rainfall, and modified precipitation variability (including a 1000-year extreme drought event followed by heavy rainfall) over the growing season in two consecutive years for a species-rich temperate grassland ecosystem. The average onset of flowering (over 2 years) was significantly advanced 3.1 days by winter warming and 1.5 days by summer warming compared to control. Early flowering species responded to seasonal warming in both years, while late-flowering species responded in only 1 year to summer warming. The average onset of early flowering species was significantly advanced, 4.9 days by winter warming and 2.3 days by summer warming. Species-specific analysis showed that even within the early flowering community there were divergences. A positive correlation between plant height and shift in flowering onset was detected under winter warming (R2 = 0.20, p = 0.005). The average onsets of early and late flowering community were affected by neither winter rain nor growing season precipitation variability. Seasonal differences in warming, and particularly winter warming, might alter community dynamics among early and late flowering species which can cause shifts in the seasonal performances of temperate ecosystems.
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Andrade C, Leite SM, Santos JA. 2012. Temperature extremes in Europe: overview of their driving atmospheric patterns. Nat Hazards Earth Syst Sci 12:1671–91.
Badeck FW, Bondeau A, Böttcher K, Doktor D, Lucht W, Schaber J, Sitch S. 2004. Responses of spring phenology to climate change. New Phytol 162:295–309.
Bates D, Maechler M, Bolker B, Walker S. 2015. Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67:1–48.
Bloor JMG, Pichon P, Falcimagne R, Leadley P, Soussana JF. 2010. Effects of warming, summer drought, and CO2 enrichment on aboveground biomass production, flowering phenology, and community structure in an upland grassland ecosystem. Ecosystems 13:888–900.
CaraDonna PJ, Iler AM, Inouye DW. 2014. Shifts in flowering phenology reshape a subalpine plant community. Proc Natl Acad Sci U S A 111:4916–21.
Chmielewski F, Rötzer T. 2001. Response of tree phenology to climate change across Europe. Agric For Meteorol 108:101–12.
Cleland EE, Chiariello NR, Loarie SR, Mooney HA, Field CB. 2006. Diverse responses of phenology to global changes in a grassland ecosystem. Proc Natl Acad Sci U S A 103:13740–4.
Cook BI, Wolkovich EM, Parmesan C. 2012. Divergent responses to spring and winter warming drive community level flowering trends. Proc Natl Acad Sci USA 109:9000–5.
Cornelius C, Heinichen J, Drösler M, Menzel A. 2014. Impacts of temperature and water table manipulation on grassland phenology. Appl Veg Sci 17:625–35.
Deutscher Wetterdienst. (2015) Zahlen Und Fakten Zum Klimawandel in Deutschland. pp. 1–36. Source: http://www.dwd.de/DE/presse/pressekonferenzen/DE/2015/PK_10_03-2015/zundf_zur_pk.pdf?__blob=publicationFile&v=3.
Fitter A, Fitter R. 2002. Rapid changes in flowering time in British plants. Science 296:1689–91.
Glaser B, Jentsch A, Kreyling J, Beierkuhnlein C. 2013. Soil-moisture change caused by experimental extreme summer drought is similar to natural inter-annual variation in a loamy sand in Central Europe. J Plant Nutr Soil Sci 176:27–34.
Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A. 2005. Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–78.
Hope RM. 2013. Rmisc: Rmisc: Ryan Miscellaneous. R package version 1.5. https://CRAN.R-project.org/package=Rmisc.
Hothorn T, Bretz F, Westfall P. 2008. Simultaneous inference in general parametric models. Biom J 50:346–63.
Hovenden MJ, Wills KE, Vander Schoor JK, Williams AL, Newton PCD. 2008. Flowering phenology in a species-rich temperate grassland is sensitive to warming but not elevated CO2. New Phytol 178:815–22.
IPCC. 2013. Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change [Stocker TF, Qin D, Plattner GK, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds.)] Cambridge: Cambridge University Press.
Isbell F, Craven D, Conolly J, Loreau M, Schmid B, Beierkuhnlein C, Bezemer TM, Bonin C, Bruelheide H, de Luca E, Ebeling A, Griffin JN, Guo Q, Hautier Y, Hector A, Jentsch A, Kreyling J, Lanta V, Manning P, Meyer ST, Mori AS, Naeem S, Niklaus P, Polley HW, Reich PB, Roscher C, Seabloom EW, Smith MD, Thakur MP, Tilman D, Tracy BF, van der Putten WH, von Ruinven J, Weigelt A, Weisser WW, Wilsey B, Eisenhauer N. 2015. Biodiversity increases the resistance of ecosystem productivity to climate extremes. Nature 526:574–7.
Jacob D. 2009. Regionalisierte Szenarien des Klimawandels. Raumforsch Raumordn 67:89–96.
Jäger EJ. 2011. Rothmaler-Exkursionsflora von Deutschland, Gefäßpflanzen: Grundband. 20th add. Heidelberg: Spektrum Akademischer Verlag
Jentsch A, Beierkuhnlein C. 2010. Simulating the future—responses of ecosystems, key species, and European provenances to expected climatic trends and events. Nov Acta Leopoldina NF 384:89–98.
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 Chang Biol 15:837–49.
Kattge J, Diaz S, Lavorel S, Prentice IC, Leadley P, Bönisch G, Garnier E, Westoby M, Reich PB, Wright IJ, Cornelissen JHC, Violle C, Harrison SP, Van Bodegom PM, Reichstein M, Enquist BJ, Soudzilovskaia NA, Ackerly DD, Anand M, Atkin O, Bahn M, Baker TR, Baldocchi D, Bekker R, Blanco CC, Blonder B, Bond WJ, Bradstock R, Bunker DE, Casanoves F, Cavender-Bares J, Chambers JQ, Chapin FS, Chave J, Coomes D, Cornwell WK, Craine JM, Dobrin BH, Duarte L, Durka W, Elser J, Esser G, Estiarte M, Fagan WF, Fang J, Fernandez-Mendez F, Fidelis A, Finegan B, Flores O, Ford H, Frank D, Freschet GT, Fyllas NM, Gallagher RV, Green WA, Gutierrez AG, Hickler T, Higgins SI, Hodgson JG, Jalili A, Jansen S, Joly CA, Kerkhoff AJ, Kirkup D, Kitajima K, Kleyer M, Klotz S, Knops JMH, Kramer K, Kühn I, Kurokawa H, Laughlin D, Lee TD, Leishman M, Lens F, Lenz T, Lewis SL, Lloyd J, Llusia J, Louault F, Ma S, Mahecha MD, Manning P, Massad T, Medlyn BE, Messier J, Moles AT, Müller SC, Nadrowski K, Naeem S, Niinemets Ü, Nöllert S, Nüske A, Ogaya R, Oleksyn J, Onipchenko VG, Onoda Y, Ordonez J et al. 2011. TRY—a global database of plant traits. Glob Chang Biol 17:2905–35.
Körner C, Basler D. 2010. Phenology under global warming. Science 327:1461–2.
Kotlarski S, Keuler K, Christensen OB, Colette A, Déqué M, Gobiet A, Goergen K, Jacob D, Lüthi D, Van Meijgaard E, Nikulin G, Schär C, Teichmann C, Vautard R, Warrach-Sagi K, Wulfmeyer V. 2014. Regional climate modeling on European scales: a joint standard evaluation of the EURO-CORDEX RCM ensemble. Geosci Model Dev 7:1297–333.
Kreyling J, Henry H. 2011. Vanishing winters in Germany: soil frost dynamics and snow cover trends, and ecological implications. Clim Res 46:269–76.
McKane RB, Grigal DF, Russelle MP. 1990. Spatiotemporal differences in 15 N uptake and the organization of an old-field plant community. Ecology 71:1126–32.
Memmott J, Craze PG, Waser NM, Price MV. 2007. Global warming and the disruption of plant-pollinator interactions. Ecol Lett 10:710–17.
Menzel A, Fabian P. 1999. Growing season extended in Europe. Nature 397:659.
Menzel A, Sparks TH, Estrella N, Koch E, Aaasa A, Ahas R, Alm-Kübler K, Bissolli P, Braslavská O, Briede A, Chmielewski FM, Crepinsek Z, Curnel Y, Dahl Å, Defila C, Donnelly A, Filella Y, Jatczak K, Måge F, Mestre A, Nordli Ø, Peñuelas J, Pirinen P, Remišová V, Scheifinger H, Striz M, Susnik A, Van Vliet AJH, Wielgolaski FE, Zach S, Zust A. 2006. European phenological response to climate change matches the warming pattern. Glob Chang Biol 12:1969–76.
Moore LM, Lauenroth WK. 2017. Differential effects of temperature and precipitation on early- vs. late-flowering species. Ecosphere 8:e01819.
Morales M, R Development Core Team. 2012. sciplot: Scientific graphing functions for factorial designs. R package version 1.1-0. https://CRAN.R-project.org/package=sciplot.
Nagy L, Kreyling J, Gellesch E, Beierkuhnlein C, Jentsch A. 2013. Recurring weather extremes alter the flowering phenology of two common temperate shrubs. Int J Biometeorol 57:579–88.
Ovaskainen O, Skorokhodova S, Yakovleva M, Sukhov A, Kutenkov A, Kutenkova N, Shcherbakov A, Meyke E, Delgado MDM. 2013. Community-level phenological response to climate change. Proc Natl Acad Sci USA 110:13434–9.
Parmesan C, Yohe G. 2003. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42.
R Core Team. 2015. R 3.2.1 (code name ‘World-Famous Astronaut’): A language and environment for statistical computing. R Foundation for Statistical Computing.
Root TL, Price JT, Hall KR, Schneider SH, Rosenzweig C, Pounds JA. 2003. Fingerprints of global warming on wild animals and plants. Nature 421:57–60.
Saavedra F, Inouye DW, Price MV, Harte J. 2003. Changes in flowering and abundance of Delphinium nuttallianum (Ranunculaceae) in response to a subalpine climate warming experiment. Glob Chang Biol 9:885–94.
Santandreu M, Lloret F. 1999. Effect of flowering phenology and habitat on pollen limitation in Erica multiflora. Can J Bot 77:734–43.
Scaven VL, Rafferty NE. 2013. Physiological effects of climate change on flowering plants and insect pollinators and potential consequences for their interactions. Curr Zool 59:418–26.
Sherry RA, Zhou X, Gu S, Arnone JA, Schimel DS, Verburg PS, Wallace LL, Luo Y. 2007. Divergence of reproductive phenology under climate warming. Proc Natl Acad Sci USA 104:198–202.
Vautard R, Gobiet A, Jacob D, Belda M, Colette A, Déqué M, Fernández J, García-Díez M, Goergen K, Güttler I, Halenka T, Karacostas T, Katragkou E, Keuler K, Kotlarski S, Mayer S, van Meijgaard E, Nikulin G, Patarčić M, Scinocca J, Sobolowski S, Suklitsch M, Teichmann C, Warrach-Sagi K, Wulfmeyer V, Yiou P. 2013. The simulation of European heat waves from an ensemble of regional climate models within the EURO-CORDEX project. Clim Dyn 41:2555–75.
Vautard R, Gobiet A, Sobolowski S, Kjellström E, Stegehuis A, Watkiss P, Mendlik T, Landgren O, Nikulin G, Teichmann C, Jacob D. 2014. The European climate under a 2°C global warming. Environ Res Lett 9:34006.
Walter J, Jentsch A, Beierkuhnlein C, Kreyling J. 2013. Ecological stress memory and cross stress tolerance in plants in the face of climate extremes. Environ Exp Bot 94:3–8.
Wickham H. 2009. ggplot2: Elegant graphics for data analysis. New York: Springer-Verlag. p 2009.
Wolf AA, Zavaleta ES, Selmants PC. 2017. Flowering phenology shifts in response to biodiversity loss. Proc Natl Acad Sci U S A 114:3463–8.
Wolkovich EM, Jonathan Davies T, Schaefer H, Cleland EE, Cook BI, Travers SE, Willis CG, Davis CC. 2013. Temperature-dependent shifts in phenology contribute to the success of exotic species with climate change. Am J Bot 100:1407–21.
Zolina O. 2012. Changes in intense precipitation in Europe. In: Kundzewicz ZW, Ed. Changes in flood risk in Europe. London: IAHS Special Publication. p 97–120.
Acknowledgements
The research was funded by the German Science Foundation (DFG JE 282/6-1) and by the “Bavarian Climate Programme 2020” of the Bavarian State Ministry of Sciences, Research and the Arts within the FORKAST research cooperation “Impact of Climate on Ecosystems and Climatic Adaptation Strategies.” Arfin Khan was supported by the German Academic Exchange Service (DAAD). The authors also acknowledge the financial support by the German Federal Ministry of Education and Research (BMBF) in the framework of the BonaRes project SUSALPS (project number: 031B0027C). A special thanks to Peter Wilfahrt for native English editing. We also thank Roman Hein and all actors of the EVENT experiments at the University of Bayreuth for setting up and maintaining the experimental facilities and for helping during field data collection.
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AJ, CB and JK designed the study. SB and SV performed the research. MASAK analyzed the data and prepared all figures and tables. MASAK wrote the paper with contributions from all authors.
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Arfin Khan, M.A.S., Beierkuhnlein, C., Kreyling, J. et al. Phenological Sensitivity of Early and Late Flowering Species Under Seasonal Warming and Altered Precipitation in a Seminatural Temperate Grassland Ecosystem. Ecosystems 21, 1306–1320 (2018). https://doi.org/10.1007/s10021-017-0220-2
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DOI: https://doi.org/10.1007/s10021-017-0220-2