Phenological Sensitivity of Early and Late Flowering Species Under Seasonal Warming and Altered Precipitation in a Seminatural Temperate Grassland Ecosystem
- 475 Downloads
- 4 Citations
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.
Keywords
climatic extreme drought ecosystem productivity mesic plant–climate interactions phenology plant trait rain seasonal climate change temperatureNotes
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.
Supplementary material
References
- 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.CrossRefGoogle Scholar
- 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.CrossRefGoogle Scholar
- Bates D, Maechler M, Bolker B, Walker S. 2015. Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67:1–48.CrossRefGoogle Scholar
- 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.CrossRefGoogle Scholar
- 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.CrossRefGoogle Scholar
- Chmielewski F, Rötzer T. 2001. Response of tree phenology to climate change across Europe. Agric For Meteorol 108:101–12.CrossRefGoogle Scholar
- 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.CrossRefGoogle Scholar
- 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.CrossRefGoogle Scholar
- 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.CrossRefGoogle Scholar
- 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.CrossRefGoogle Scholar
- 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.CrossRefGoogle Scholar
- 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.CrossRefGoogle Scholar
- 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.CrossRefGoogle Scholar
- 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.CrossRefGoogle Scholar
- 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.Google Scholar
- 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.CrossRefGoogle Scholar
- Jacob D. 2009. Regionalisierte Szenarien des Klimawandels. Raumforsch Raumordn 67:89–96.CrossRefGoogle Scholar
- Jäger EJ. 2011. Rothmaler-Exkursionsflora von Deutschland, Gefäßpflanzen: Grundband. 20th add. Heidelberg: Spektrum Akademischer VerlagGoogle Scholar
- 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.Google Scholar
- 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.CrossRefGoogle Scholar
- 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.CrossRefGoogle Scholar
- Körner C, Basler D. 2010. Phenology under global warming. Science 327:1461–2.CrossRefGoogle Scholar
- 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.CrossRefGoogle Scholar
- Kreyling J, Henry H. 2011. Vanishing winters in Germany: soil frost dynamics and snow cover trends, and ecological implications. Clim Res 46:269–76.CrossRefGoogle Scholar
- 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.CrossRefGoogle Scholar
- Memmott J, Craze PG, Waser NM, Price MV. 2007. Global warming and the disruption of plant-pollinator interactions. Ecol Lett 10:710–17.CrossRefGoogle Scholar
- Menzel A, Fabian P. 1999. Growing season extended in Europe. Nature 397:659.CrossRefGoogle Scholar
- 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.CrossRefGoogle Scholar
- Moore LM, Lauenroth WK. 2017. Differential effects of temperature and precipitation on early- vs. late-flowering species. Ecosphere 8:e01819.CrossRefGoogle Scholar
- 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.CrossRefGoogle Scholar
- 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.CrossRefGoogle Scholar
- Parmesan C, Yohe G. 2003. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42.CrossRefGoogle Scholar
- 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.Google Scholar
- 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.CrossRefGoogle Scholar
- 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.CrossRefGoogle Scholar
- Santandreu M, Lloret F. 1999. Effect of flowering phenology and habitat on pollen limitation in Erica multiflora. Can J Bot 77:734–43.Google Scholar
- 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.CrossRefGoogle Scholar
- 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.CrossRefGoogle Scholar
- 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.CrossRefGoogle Scholar
- 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.CrossRefGoogle Scholar
- 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.CrossRefGoogle Scholar
- Wickham H. 2009. ggplot2: Elegant graphics for data analysis. New York: Springer-Verlag. p 2009.CrossRefGoogle Scholar
- 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.CrossRefGoogle Scholar
- 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.CrossRefGoogle Scholar
- 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.CrossRefGoogle Scholar