Register      Login
Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
RESEARCH ARTICLE

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
+ Author Affiliations
- Author Affiliations

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: Mark.Hovenden@utas.edu.au

Australian Journal of Botany 56(8) 630-643 https://doi.org/10.1071/BT08142
Submitted: 6 August 2008  Accepted: 3 November 2008   Published: 15 December 2008

Abstract

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.


Acknowledgements

We thank the Australian Federal Department of Defence for access to the Pontville Small Arms Range Complex. This project was supported by the Australian Research Council Discovery Projects scheme.


References


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. open url image1

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.
Crossref | GoogleScholarGoogle Scholar | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | open url image1

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. open url image1

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.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | open url image1

Crepinsek Z, Kajfez-Bogataj L, Bergant K (2006) Modelling of weather variability effect on fitophenology. Ecological Modelling 194, 256–265.
Crossref | GoogleScholarGoogle Scholar | open url image1

Day RW, Quinn GP (1989) Comparisons of treatments after an analysis of variance in ecology. Ecological Monographs 59, 433–463.
Crossref | GoogleScholarGoogle Scholar | open url image1

De Valpine P, Harte J (2001) Plant responses to experimental warming in a montane meadow. Ecology 82, 637–648. open url image1

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.
Crossref | GoogleScholarGoogle Scholar | open url image1

Fitter AH, Fitter RSR (2002) Rapid changes in flowering time in British plants. Science 296, 1689–1691.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

García LV (2003) Controlling the false discovery rate in ecological research. Trends in Ecology & Evolution 18, 553–554.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hendrey GR, Lewin KF, Nagy J (1993) Free air carbon dioxide enrichment: development, progress, results. Vegetatio 104–105, 17–31.
Crossref | GoogleScholarGoogle Scholar | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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. open url image1

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.
Crossref | GoogleScholarGoogle Scholar | open url image1

Keeling CD, Chin JFS, Whorf TP (1996) Increased activity of northern vegetation inferred from atmospheric CO2 measurements. Nature 382, 146–149.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Keller F, Körner C (2003) The role of photoperiodism in alpine plant development. Arctic, Antarctic, and Alpine Research 35, 361–368.
Crossref | GoogleScholarGoogle Scholar | open url image1

MacDougall AS, Turkington R (2005) Are invasive species the drivers or passengers of change in degraded ecosystems? Ecology 86, 42–55.
Crossref | GoogleScholarGoogle Scholar | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | open url image1

Penuelas J, Filella I (2001) Phenology—Responses to a warming world. Science 294, 793–795.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | open url image1

Perneger TV (1998) What’s wrong with Bonferroni adjustments. BMJ 316, 1236–1238.
CAS | PubMed |
open url image1

Price MV, Waser NM (1998) Effects of experimental warming on plant reproductive phenology in a subalpine meadow. Ecology 79, 1261–1271. open url image1

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.
Crossref | GoogleScholarGoogle Scholar | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

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.
CAS | PubMed |
open url image1

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.
Crossref | GoogleScholarGoogle Scholar | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Springer CJ, Ward JK (2007) Flowering time and elevated atmospheric CO2. New Phytologist 176, 243–255.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | open url image1

Stewart J, Potvin C (1996) Effects of elevated CO2 on an artificial grassland community: competition, invasion and neighbourhood growth. Functional Ecology 10, 157–166.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sultan SE (2001) Phenotypic plasticity for fitness components in Polygonum species of contrasting ecological breadth. Ecology 82, 328–343. open url image1

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.
Crossref | GoogleScholarGoogle Scholar | open url image1

Verhoeven KJF, Simonsen KL, Mcintyre LM (2005) Implementing false discovery rate control: increasing your power. Oikos 108, 643–647.
Crossref | GoogleScholarGoogle Scholar | open url image1

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.
Crossref |
open url image1

Waite TA, Campbell LG (2006) Controlling the false discovery rate and increasing statistical power in ecological studies. Ecoscience 13, 439–442.
Crossref | GoogleScholarGoogle Scholar | open url image1

Walther GR (2004) Plants in a warmer world. Perspectives in Plant Ecology, Evolution and Systematics 6, 169–185.
Crossref | GoogleScholarGoogle Scholar | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | open url image1