Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems

Elevated CO2 and warming impacts on flowering phenology in a southern Australian grassland are related to flowering time but not growth form, origin or longevity

Mark J. Hovenden A C , Amity L. Williams A , Jane Kongstad Pedersen B , Jacqueline K. Vander Schoor A and Karen E. Wills A

A School of Plant Science, University of Tasmania, Hobart, Tasmania 7001, Australia.

B Forest and Landscape Denmark, University of Copenhagen, Hørsholm, Denmark.

C Corresponding author. Email:

Australian Journal of Botany 56(8) 630-643
Submitted: 6 August 2008  Accepted: 3 November 2008   Published: 15 December 2008


Flowering is a critical stage in plant life cycles, and changes in phenology might alter processes at the species, community and ecosystem levels. Therefore, likely flowering-time responses to global-change drivers are needed for predictions of global-change impacts on natural and managed ecosystems. Predicting responses of species to global changes would be simplified if functional, phylogenetic or biogeographical traits contributed substantially to a species’ response. Here we investigate the role of growth form (grass, graminoid, forb, subshrub), longevity (annual, perennial), origin (native, exotic) and flowering time in determining the impact of elevated [CO2] (550 μmol mol-1) and infrared warming (mean warming of +2°C) on flowering times of 31 co-occurring species of a range of species-types in a temperate grassland in 2004, 2005 and 2007. Warming reduced time to first flowering by an average of 20.3 days in 2004, 2.1 days in 2005 and 7.6 days in 2007; however, the response varied among species and was unrelated to growth form, origin or longevity. Elevated [CO2] did not alter flowering times; neither was there any [CO2] by species-type interaction. However, both warming and elevated [CO2] tended to have a greater effect on later-flowering species, with time to first flowering of later-flowering species being reduced by both elevated [CO2] (P < 0.001) and warming (P < 0.001) to a greater extent than that of earlier-flowering species. These results have ramifications for our predictions of community and ecosystem interactions in native grasslands in response to global change.


Arft AM Walker MD Gurevitch J Alatalo JM Bret-Harte MS Dale M Diemer M Gugerli F Henry GHR Hollister RD Jónsdóttir IS Laine K Lévesque E Marion GM Molau U Mølgaard P Nordenhüll U Raszhivin V Robinson CH Starr G Stenström A Stenström M Totland Ø Turner PL Walker LJ Webber PJ Welker JM Wookey PA 1999 Responses of tundra plants to experimental warming: meta-analysis of the international tundra experiment. Ecological Monographs 69 491 511

Badeck FW Bondeau A Bottcher K Doktor D Lucht W Schaber J Sitch S 2004 Responses of spring phenology to climate change. New Phytologist 162 295 309

Beaubien EG Hall-Beyer M 2003 Plant phenology in western Canada: trends and links to the view from space. Ecological Monitoring and Assesment 88 419 429 doi:10.1023/A:1025597829895

Benjamini Y Hochberg Y 1995 Controlling the false discovery rate—a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society: Series B 57 289 300

Brando P Ray D Nepstad D Cardinot G Curran LM Oliveira R 2006 Effects of partial throughfall exclusion on the phenology of Coussarea racemosa (Rubiaceae) in an east-central Amazon rainforest. Oecologia 150 181 189

Brearley FQ Proctor J Suriantata Nagy L Dalrymple G Voysey BC 2007 Reproductive phenology over a 10-year period in a lowland evergreen rain forest of central Borneo. Journal of Ecology 95 828 839 doi:10.1111/j.1365-2745.2007.01258.x

Buchanan AM (1999) ‘A census of the vascular plants of Tasmania.’ (Tasmanian Herbarium: Hobart)

Cleland EE Chiariello NR Loarie SR Mooney HA Field CB 2006 Diverse responses of phenology to global changes in a grassland ecosystem. Proceedings of the National Academy of Sciences, USA 103 13740 13744 doi:10.1073/pnas.0600815103

Cleland EE Chuine I Menzel A Mooney HA Schwartz MD 2007 Shifting plant phenology in response to global change. Trends in Ecology & Evolution 22 357 365 doi:10.1016/j.tree.2007.04.003

Crepinsek Z Kajfez-Bogataj L Bergant K 2006 Modelling of weather variability effect on fitophenology. Ecological Modelling 194 256 265 doi:10.1016/j.ecolmodel.2005.10.020

Day RW Quinn GP 1989 Comparisons of treatments after an analysis of variance in ecology. Ecological Monographs 59 433 463 doi:10.2307/1943075

De Valpine P Harte J 2001 Plant responses to experimental warming in a montane meadow. Ecology 82 637 648

Dunne JA Harte J Taylor KJ 2003 Subalpine meadow flowering phenology responses to climate change: integrating experimental and gradient approaches. Ecological Monographs 73 69 86

Fitter AH Fitter RSR 2002 Rapid changes in flowering time in British plants. Science 296 1689 1691 doi:10.1126/science.1071617

García LV 2003 Controlling the false discovery rate in ecological research. Trends in Ecology & Evolution 18 553 554 doi:10.1016/j.tree.2003.08.011

Hendrey GR Lewin KF Nagy J 1993 Free air carbon dioxide enrichment: development, progress, results. Vegetatio 104–105 17 31 doi:10.1007/BF00048142

Hendrey GR Ellsworth DS Lewin KF Nagy J 1999 A free-air enrichment system for exposing tall forest vegetation to elevated atmospheric CO2. Global Change Biology 5 293 309 doi:10.1046/j.1365-2486.1999.00228.x

Holtum JAM Winter K 2003 Photosynthetic CO2 uptake in seedlings of two tropical tree species exposed to oscillating elevated concentrations of CO2. Planta 218 152 158 doi:10.1007/s00425-003-1089-1

Hovenden MJ Miglietta F Zaldei A Vander Schoor JK Wills KE Newton PCD 2006 The TasFACE climate change impacts experiment: design and performance of combined elevated CO2 and temperature enhancement in a native Tasmanian grassland. Australian Journal of Botany 54 1 10 doi:10.1071/BT04194

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 Phytologist 178 815 822 doi:10.1111/j.1469-8137.2008.02419.x

Johnston FM Pickering CM 2006 Phenology of the environmental weed Achillea millefolium (Asteraceae) along altitudinal and disturbance gradients in the Snowy Mountains, Australia. Nordic Journal of Botany 24 148 160

Keatley MR Fletcher TD Hudson IL Ades PK 2002 Phenological studies in Australia: potential application in historical and future climate analysis. International Journal of Climatology 22 1769 1780

Keeling CD Chin JFS Whorf TP 1996 Increased activity of northern vegetation inferred from atmospheric CO2 measurements. Nature 382 146 149 doi:10.1038/382146a0

Keller F Körner C 2003 The role of photoperiodism in alpine plant development. Arctic, Antarctic, and Alpine Research 35 361 368 doi:10.1657/1523-0430(2003)035[0361:TROPIA]2.0.CO;2

MacDougall AS Turkington R 2005 Are invasive species the drivers or passengers of change in degraded ecosystems? Ecology 86 42 55 doi:10.1890/04-0669

Miglietta F Peressotti A Primo Vacari F Zaldei A De Angelis P Scarscia Mugnozza G 2001 Free air CO2 enrichment (FACE) of a poplar plantation: the POPFACE fumigation system. New Phytologist 150 465 476 doi:10.1046/j.1469-8137.2001.00115.x

Mooney HA , Hobbs RJ (2000) ‘Invasive species in a changing world.’ (Island Press: Washington, DC)

Moran MD 2003 Arguments for rejecting the sequential Bonferroni in ecological studies. Oikos 100 403 405 doi:10.1034/j.1600-0706.2003.12010.x

Myneni RB Keeling CD Tucker CJ Asrar G Nemani RR 1997 Increased plant growth in the northern high latitudes from 1981 to 1991. Nature 386 698 702 doi:10.1038/386698a0

Osborne CP Chuine I Viner D Woodward FI 2000 Olive phenology as a sensitive indicator of future climatic warming in the Mediterranean. Plant, Cell & Environment 23 701 710 doi:10.1046/j.1365-3040.2000.00584.x

Penuelas J Filella I 2001 Phenology—Responses to a warming world. Science 294 793 795 doi:10.1126/science.1066860

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 doi:10.1046/j.1365-2486.2002.00489.x

Penuelas J Filella I Zhang XY Llorens L Ogaya R Lloret F Comas P Estiarte M Terradas J 2004 Complex spatiotemporal phenological shifts as a response to rainfall changes. New Phytologist 161 837 846 doi:10.1111/j.1469-8137.2004.01003.x

Perneger TV 1998 What’s wrong with Bonferroni adjustments. BMJ 316 1236 1238

Price MV Waser NM 1998 Effects of experimental warming on plant reproductive phenology in a subalpine meadow. Ecology 79 1261 1271

Primack D Imbres C Primack RB Miller-Rushing AJ Del Tredici P 2004 Herbarium specimens demonstrate earlier flowering times in response to warming in Boston. American Journal of Botany 91 1260 1264

Randerson JT Field CB Fung IY Tans PP 1999 Increases in early season ecosystem uptake explain recent changes in the seasonal cycle of atmospheric CO2 at high northern latitudes. Geophysical Research Letters 26 2765 2768 doi:10.1029/1999GL900500

Reich PB Tilman D Craine J Ellsworth D Tjoelker MG Knops J Wedin D Naeem S Bahauddin D Goth J Bengston W Lee TD 2001 Do species and functional groups differ in acquisition and use of C, N and water under varying atmospheric CO2 and N availability regimes? A field test with 16 grassland species. New Phytologist 150 435 448 doi:10.1046/j.1469-8137.2001.00114.x

Rivera G Borchert R 2001 Induction of flowering in tropical trees by a 30-min reduction in photoperiod: evidence from field observations and herbarium specimens. Tree Physiology 21 201 212

Roumet C Garnier E Suzor H Salager J Roy J 2000 Short and long-term responses of whole-plant gas exchange to elevated CO2 in four herbaceous species. Environmental and Experimental Botany 43 155 169

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 doi:10.1046/j.1365-2486.2003.00635.x

SAS Institute Inc. (2003) ‘SAS/STAT user’s guide, version 9.1.’ (SAS Publishing: Cary, NC)

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 doi:10.1073/pnas.0605642104

Springer CJ Ward JK 2007 Flowering time and elevated atmospheric CO2. New Phytologist 176 243 255 doi:10.1111/j.1469-8137.2007.02196.x

Stefanescu C Penuelas J Filella I 2003 Effects of climatic change on the phenology of butterflies in the northwest Mediterranean Basin. Global Change Biology 9 1494 1506 doi:10.1046/j.1365-2486.2003.00682.x

Stewart J Potvin C 1996 Effects of elevated CO2 on an artificial grassland community: competition, invasion and neighbourhood growth. Functional Ecology 10 157 166 doi:10.2307/2389839

Sultan SE 2001 Phenotypic plasticity for fitness components in Polygonum species of contrasting ecological breadth. Ecology 82 328 343

Suzuki S Kudo G 2000 Responses of alpine shrubs to simulated environmental change during three years in the mid-latitude mountain, northern Japan. Ecography 23 553 564

Verhoeven KJF Simonsen KL Mcintyre LM 2005 Implementing false discovery rate control: increasing your power. Oikos 108 643 647 doi:10.1111/j.0030-1299.2005.13727.x

Vidiella PE Armesto JJ Gutierrez JR 1999 Vegetation changes and sequential flowering after rain in the southern Atacama Desert. Journal of Arid Environments 43 449 458

Waite TA Campbell LG 2006 Controlling the false discovery rate and increasing statistical power in ecological studies. Ecoscience 13 439 442

Walther GR 2004 Plants in a warmer world. Perspectives in Plant Ecology, Evolution and Systematics 6 169 185 doi:10.1078/1433-8319-00076

Walther GR Post E Convey P Menzel A Parmesan C Beebee TJC Fromentin JM Hoegh-Guldberg O Bairlein F 2002 Ecological responses to recent climate change. Nature 416 389 395 doi:10.1038/416389a

Williams AL Wills KE Janes JK Vander Schoor JK Newton PCD Hovenden MJ 2007 Warming and free air CO2 enrichment alter demographics in four co-occurring grassland species. New Phytologist 176 365 374 doi:10.1111/j.1469-8137.2007.02170.x

Zhou LM Tucker CJ Kaufmann RK Slayback D Shabanov NV Myneni RB 2001 Variations in northern vegetation activity inferred from satellite data of vegetation index during 1981 to 1999. Journal of Geophysical Research—Atmospheres 106 20069 20083 doi:10.1029/2000JD000115

Export Citation Cited By (8)