Changes in leaf phenology of three European oak species in response to experimental climate change.
*Because the phenology of trees is strongly driven by environmental factors such as temperature, climate change has already altered the vegetative and reproductive phenology of many species, especially in the temperate zone. Here, we aimed to determine whether projected levels of warming for the upcoming decades will lead to linear changes in the phenology of trees or to more complex responses. *We report the results of a 3-yr common garden experiment designed to study the phenological response to artificial climate change, obtained through experimental warming and reduced precipitation, of several populations of three European oaks, two deciduous species (Quercus robur, Quercus pubescens) and one evergreen species (Quercus ilex), in a Mediterranean site. *Experimental warming advanced the seedlings' vegetative phenology, causing a longer growing season and higher mortality. However, the rate of advancement of leaf unfolding date was decreased with increasing temperature. Conversely, soil water content did not affect the phenology of the seedlings or their survival. *Our results show that the phenological response of trees to climate change may be nonlinear, and suggest that predictions of phenological changes in the future should not be built on extrapolations of current observed trends.
Morin
Xavier
X
Centre d'Ecologie Fonctionnelle et Evolutive, Equipe BIOFLUX, CNRS, 1919, route de Mende, F-34293 Montpellier Cedex 5, France.|Present address: Forest Ecology, Institute of Terrestrial Ecosystems, Department of Environmental Sciences, Swiss Federal Institute of Technology ETH, Universitätstrasse 22, CH-8092 Zürich, Switzerland.
Roy
Jacques
J
Centre d'Ecologie Fonctionnelle et Evolutive, Equipe BIOFLUX, CNRS, 1919, route de Mende, F-34293 Montpellier Cedex 5, France.
Sonié
Laurette
L
Centre d'Ecologie Fonctionnelle et Evolutive, Equipe BIOFLUX, CNRS, 1919, route de Mende, F-34293 Montpellier Cedex 5, France.
Chuine
Isabelle
I
Centre d'Ecologie Fonctionnelle et Evolutive, Equipe BIOFLUX, CNRS, 1919, route de Mende, F-34293 Montpellier Cedex 5, France.
D000388:Air; D000704:Analysis of Variance; D016922:Cellular Senescence; D057231:Climate Change; D005060:Europe; D006358:Hot Temperature; D008954:Models, Biological; D018515:Plant Leaves / Q000033:anatomy & histology / Q000166:cytology / Q000502:physiology*; D029963:Quercus / Q000254:growth & development / Q000502:physiology*; D011891:Rain; D012621:Seasons; D012987:Soil / Q000032:analysis; D014867:Water / Q000032:analysis
D012987:Soil; D014867:Water
Ahas R, Aasa A, Menzel A, Fedotova VG, Scheifinger H. 2002. Changes in European spring phenology. International Journal of Climatology 22: 1727-1738.
Ahas R, Jaagus J, Aasa A. 2000. The phenological calendar of Estonia and its correlation with mean air temperature. International Journal of Biometeorology 44: 159-166.
Ainsworth EA, Long SP. 2005. What have we learned from 15 years of free-air CO2 enrichment (face)? A meta-analytic review of the responses of photosynthesis, canopy. New Phytologist 165: 351-371.
Arft AM, Walker MD, Gurevitch J, Alatalo JM, Bret-Harte MS, Dale M, Diemer M, Gugerli F, Henry GHR, Jones MH et al. 1999. Responses of tundra plants to experimental warming: meta-analysis of the international tundra experiment. Ecological Monographs 69: 491-511.
Asshoff R, Zotz G, Korner C. 2006. Growth and phenology of mature temperate forest trees in elevated CO2. Global Change Biology 12: 848-861.
Betts RA, Cox PM, Lee SE, Woodward FI. 1997. Contrasting physiological and structural vegetation feedbacks in climate change simulations. Nature 387: 796-799.
Beuker E. 1994. Adaptation to climatic changes of the timing of bud burst in populations of Pinus sylvestris (L.) and Picea abies (L.) karst. Tree Physiology 14: 961-970.
Cannell MGR. 1989. Chilling, thermal time and the dates of flowering of trees. In: Wright CJ, ed. Manipulation of fruiting. London, UK: Butterworth & Co, 99-113.
Cannell MGR, Palutikof JP, Sparks T. 1999. Indicators of climate change in the UK. London, UK: DETR.
Cattadori IM, Haydon DT, Hudson PJ. 2005. Parasites and climate synchronize red grouse populations. Nature 433: 737-741.
Chapin FS III, Matson PA, Mooney HA. 2002. Principles of terrestrial ecosystem ecology. New York, NY, USA: Springer.
Doi H, Takahashi M, Katano I. 2010. Genetic diversity increases regional variation in phenological dates in response to climate change. Global Change Biology 16: 373-379.
Ducousso A, Guyon J, Krémer A. 1996. Latitudinal and altitudinal variation of bud burst in western populations of sessile oak (Quercus petraea (matt) liebl). Annals of Forest Science 53: 775-782.
Edwards M, Richardson AJ. 2004. Impact of climate change on marine pelagic phenology and trophic mismatch. Nature 430: 881-884.
Franks SJ, Sim S, Weis AE. 2007. Rapid evolution of flowering time by an annual plant in response to a climate fluctuation. Proceedings of the National Academy of Sciences, USA 104: 1278-1282.
Gordo O, Sanz JJ. 2005. Phenology and climate change: a long-term study in a Mediterranean locality. Oecologia 146: 484-495.
Guak S, Olsyzk DM, Fuchigami LH, Tingey DT. 1998. Effects of elevated CO2 and temperature on cold hardiness and spring bud burst and growth in Douglas-fir (Pseudotsuga menziessi). Tree Physiology 18: 671-679.
Hampe A, Petit RJ. 2005. Conserving biodiversity under climate change: the rear edge matters. Ecology Letters 8: 461-467.
Hänninen H. 1987. Effects of temperature on dormancy release in woody plants: implications of prevailing models. Silva Fennica 21: 279-299.
Hollister RD, Webber PJ, Bay C. 2005. Plant response to temperature in northern Alaska: implications for predicting vegetation change. Ecology 86: 1562-1570.
Howe GT, Aitken SN, Neale DB, Jermstad KD, Wheeler NC, Chen THH. 2003. From genotype to phenotype: unraveling the complexities of cold adaptation in forest trees. Canadian Journal of Botany 81: 1247-1266.
Ihaka R, Gentleman R. 1996. R: a language for data analysis and graphics. Journal of Computational and Graphical Statistics 5: 299-314.
IPCC. 2001. Climate change 2001: impacts, adaptation and vulnerability. Contribution of the working group II to the third assessment report of IPCC. Cambridge, UK/New York, USA: Cambridge University Press.
IPCC. 2007. 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, UK/New York, USA: Cambridge University Press.
Jalas J, Suominen J. 19721999. Atlas florae europaeae. Distribution of vascular plants in Europe. Vols 1-12. Helsinki, Finland: The Committee for Mapping the Flora of Europe & Societas Biologica Fennica Vanamo.
Jensen JS, Hansen JK. 2008. Geographical variation in phenology of Quercus petraea (matt.) Liebl and Quercus robur L. Oak grown in a greenhouse. Scandinavian Journal of Forest Research 23: 179-188.
Jones MH, Bay C, Nordenhall U. 1997. Effects of experimental warming on arctic willows (Salix spp.): a comparison of responses from the Canadian High Arctic, Alaskan Arctic, and Swedish Subarctic. Global Change Biology 3: 55-60.
Jump AS, Penuelas J. 2005. Running to stand still: adaptation and the response of plants to rapid climate change. Ecology Letters 8: 1010-1020.
Keeling CD, Chin JFS, Whorf TP. 1996. Increased activity of northern vegetation inferred from atmospheric CO2 measurements. Nature 382: 146-149.
Kelly CK, Chase MW, de Bruijn A, Fay MF, Woodward FI. 2003. Temperature-based population segregation in birch. Ecology Letters 6: 87-89.
Kennedy AD. 1995a. Simulated climate-change - are passive greenhouses a valid microcosm for testing the biological effects of environmental perturbations. Global Change Biology 1: 29-42.
Kennedy AD. 1995b. Temperature effects of passive greenhouse apparatus in high-latitude change experiments. Functional Ecology 9: 340-350.
Kilpelainen A, Peltola H, Rouvinen I, Kellomaki S. 2006. Dynamics of daily height growth in Scots pine trees at elevated temperature and CO2. Trees - Structure and Function 20: 16-27.
Kimball BA. 2005. Theory and performance of an infrared heater for ecosystem warming. Global Change Biology 11: 2041-2056.
Korner C, Asshoff R, Bignucolo O, Hättenschwiler S, Keel SG, Peláez-Riedl S, Pepin S, Siegwolf RTW, Zotz G. 2005. Carbon flux and growth in mature deciduous forest trees exposed to elevated CO2. Science 309: 1360-1362.
Linkosalo T, Hakkinen R, Hänninen H. 2006. Models of the spring phenology of boreal and temperate trees: is there something missing? Tree Physiology 26: 1165-1172.
Loveys BR, Egerton JJG, Ball MC. 2005. Higher daytime leaf temperatures contribute to lower freeze tolerance under elevated CO2. Plant, Cell & Environment 29: 1077-1086.
Marion GM, Henry GHR, Freckman DW, Johnstone J, Jones G, Jones MH, Levesque E, Molau U, Molgaard P, Parsons AN et al. 1997. Open-top designs for manipulating field temperature in high-latitude ecosystems. Global Change Biology 3: 20-32.
Menzel A. 2000. Trends in phenological phases in Europe between 1951 and 1996. International Journal of Biometeorology 44: 76-81.
Menzel A, Estrella N, Fabian P. 2001. Spatial and temporal variability of the phenological seasons in Germany from 1951 to 1996. Global Change Biology 7: 657-666.
Menzel A, Fabian P. 1999. Growing season extended in Europe. Nature 397: 659.
Menzel A, Sparks TH, Estrella N, Koch E, Aasa A, Aha R, Alm-Kubler K, Bissolli P, Braslavska O, Briede A et al. 2006. European phenological response to climate change matches the warming pattern. Global Change Biology 12: 1969-1976.
Morin X, Lechowicz MJ, Augspurger C, O’Keefe J, Viner D, Chuine I. 2009. Leaf phenology changes in 22 North American tree species during the 21st century. Global Change Biology 15: 961-975.
Morin X, Viner D, Chuine I. 2008. Tree species range shifts at a continental scale: new predictive insights from a process-based model. Journal of Ecology 96: 784-794.
Murray MB, Cannell MGR, Smith RI. 1989. Date of budburst of fifteen tree species in Britain following climatic warming. Journal of Applied Ecology 26: 693-700.
Myking T, Heide OM. 1995. Dormancy release and chilling requirements of buds of latitudinal ecotypes of Betula pendula and B. pubescens. Tree Physiology 15: 697-704.
Myneni RB, Keeling CD, Tucker CJ, Asrar G, Nemani RR. 1997. Increasing plant growth in the northern high latitudes from 1981 to 1991. Nature 386: 698-702.
Nakashizuka T. 2001. Species coexistence in temperate, mixed deciduous forests. Trends in Ecology & Evolution 16: 205-210.
de Noblet N. 2000. Mid-holocene greening of the Sahara: first results of the Gaim 6000 year BP experiment with two asynchronously coupled atmosphere/biome models. Climate Dynamics 16: 643-659.
Norby RJ, Hartz-Rubin JS, Verbrugge MJ. 2003. Phenological responses in maple to experimental atmospheric warming and CO2 enrichment. Global Change Biology 9: 1792-1801.
Parmesan C, Yohe G. 2003. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421: 37-42.
Penuelas J, Filella I, Comas P. 2002. Changed plant and animal life cycles from 1952 to 2000 in the Mediterranean region. Global Change Biology 8: 531-544.
Post E, Forchhammer MC, Stenseth NC, Callaghan TV. 2001. The timing of life history events in a changing climate. Proceedings of the Royal Society of London B 268: 15-23.
Price MV, Waser NM. 1998. Effects of experimental warming on plant reproductive phenology in a subalpine meadow. Ecology 79: 1261-1271.
Prieto P, Penuelas J, Niinemets U, Ogaya R, Schmidt I, Beier C, Tietema A, Sowerby A, Emmett B, Lang EK et al. 2009. Changes in the onset of shrubland species spring growth in response to an experimental warming along a north-south gradient in Europe. Global Ecology and Biogeography 18: 473-484.
Primack RB, Ibanez I, Higuchi H, Lee SD, Miller-Rushing AJ, Wilson AM, Silander JA Jr. 2009. Spatial and interspecific variability in phenological responses to warming temperatures. Biological Conservation 142: 2569-2577.
Rameau J-C, Mansion D, Dumé G. 1989. Flore forestière française. Guide écologique illustré. 1. Plaines et collines. Paris, France: Institut pour la Développement Forestier, Ministère de l’Agriculture et de la forêt.
Rameau J-C, Mansion D, Dumé G, Gauberville C. 2008. Flore forestière française. Guide écologique illustré. 3. Région méditerranéenne. Paris: Institut pour la Développement Forestier.
Repo T, Hanninen H, Kellomaki S. 1996. The effects of long-term elevation of air temperature and CO2 on the frost hardiness of Scots pine. Plant, Cell & Environment 19: 209-216.
Richardson AD, Bailey AS, Denny EG, Martin CW, O’Keefe J. 2006. Phenology of a northern hardwood forest canopy. Global Change Biology 12: 1174-1188.
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. Global Change Biology 9: 885-894.
Sarvas R. 1972. Investigations on the annual cycle of development on forest trees active period. Communicationes Instituti Forestalis Fenniae 76: 110.
Sarvas R. 1974. Investigations on the annual cycle of development of forest trees. Autumn dormancy and winter dormancy. Communicationes Instituti Forestalis Fenniae 84: 1-101.
Schär C, Jendritzky G. 2004. Hot news from summer 2003. Nature 432: 559-560.
Schwartz MD. 2003. Phenology: an integrative environmental science. Dordrecht, the Netherlands: Kluwer Academic.
Sherry RA, Zhou XH, Gu SL, Arnone JA, Schimel DS, Verburg PS, Wallace LL, Luo YQ. 2007. Divergence of reproductive phenology under climate warming. Proceedings of the National Academy of Sciences, USA 104: 198-202.
Svensson CJ, Jenkins SR, Hawkins SJ, Aberg P. 2005. Population resistance to climate change: modelling the effects of low recruitment in open populations. Global Change Biology 142: 117-126.
Van Wijk MT, Clemmensen KE, Shaver GR, Williams M, Callaghans TV, Chapin III SF, Cornelissen JHC, Gough L, Richardson SJ, Rueth H. 2003. Long-term ecosystem level experiments at Toolik Lake, Alaska, and at Abisko, Northern Sweden: generalizations and differences in ecosystem and plant responses to global change. Global Change Biology 10: 105-123.
Vitasse Y, Delzon S, Dufrêne E, Pontailler JY, Louvet JM, Kremer A, Michalet R. 2009. Leaf phenology sensitivity to temperature in European trees: do within-species populations exhibit similar responses? Agricultural and Forest Meteorology 149: 735-744.
Walker MD, Wahren CH, Hollister RD, Henry GHR, Ahlquist LE, Alatalo JM, Bret-Harte MS, Calef MP, Callaghan TV, Carroll AB et al. 2006. Plant community responses to experimental warming across the tundra biome. Proceedings of the National Academy of Sciences, USA 103: 1342-1346.
Walther G-R, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC, Fromentin J-M, Hoegh-Guldberg O, Bairlein F. 2002. Ecological responses to recent climate change. Nature 416: 389-395.