Flowering, seed production and seed mass in a species-rich temperate grassland exposed to FACE and warming
Mark J. Hovenden A D , Karen E. Wills A , Jacqueline K. Vander Schoor A , Rebecca E. Chaplin B , Amity L. Williams A , Michaela J. Nolan A and Paul C. D. Newton CA School of Plant Science, University of Tasmania, Hobart, Tas. 7001, Australia.
B School of Earth Sciences, Stanford University, Stanford, CA 94305-2210, USA.
C Land & Environmental Management, AgResearch, Palmerston North, New Zealand.
D Corresponding author. Email: Mark.Hovenden@utas.edu.au
Australian Journal of Botany 55(8) 780-794 https://doi.org/10.1071/BT07107
Submitted: 5 June 2007 Accepted: 11 October 2007 Published: 14 December 2007
Abstract
Long-term effects of climate change on plant communities must be mediated by reproductive and recruitment responses of component species. From spring 2003 until autumn 2006, we monitored flowering and seed-production responses to free air CO2 enrichment (FACE) and 2°C warming in a species-rich, nutrient-poor southern temperate grassland, by using the TasFACE experiment. There were no effects of either FACE or warming on the proportion of species flowering in any year. Flowering, seed production and seed mass were not significantly affected by FACE, warming or their interaction in most species. Some species, however, did respond significantly to simulated global changes. These responses generally were not governed by life history, but there were two distinct trends. First, warming increased the proportion of the population that flowered in perennial grasses but not in other species types. Second, flowering and seed production of both perennial woody dicots responded strongly to the interaction of FACE and warming, with Bossiaea prostrata producing most seeds in warmed FACE plots and Hibbertia hirsuta producing the most in unwarmed FACE plots. FACE increased seed mass 4-fold in the perennial C3 grass Elymus scaber (P < 0.01) but substantially reduced seed mass of the perennial C3 grass Austrodanthonia caespitosa (P < 0.02) and the perennial forb Hypochaeris radicata (P < 0.02), with the remainder of species unaffected. Our results indicate that warming and elevated CO2 had little effect on seed production in the temperate grassland ecosystem. The few significant affects there were, however, are likely to have substantial implications for community composition and structure.
Acknowledgements
We thank the Australian Federal Department of Defence for access to the Pontville Small Arms Range Complex. Thanks go to Dr Greg Jordan for much discussion and Mr Matthew Baker and Dr Alex Buchanan of the Tasmanian Herbarium for assistance with species identification. This project was supported by the Australian Research Council Discovery Projects scheme.
Ackerly D, Bazzaz F
(1995) Plant growth and reproduction along CO2 gradients: non linear responses and implications for community change. Global Change Biology 1, 199–207.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Arft AM,
Walker MD,
Gurevitch J,
Alatalo JM,
Bret-Harte MS,
Dale M,
Diemer M,
Gugerli F,
Henry GHR,
Jones MH,
Hollister RD,
Jonsdottir IS,
Laine K,
Levesque E,
Marion GM,
Molau U,
Molgaard P,
Nordenhall U,
Raszhivin V,
Robinson CH,
Starr G,
Stenstrom A,
Stenstrom M,
Totland O,
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.
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.
Berntson GM,
Rajakaruna N, Bazzaz FA
(1998) Growth and nitrogen uptake in an experimental community of annuals exposed to elevated atmospheric CO2. Global Change Biology 4, 607–626.
| Crossref | GoogleScholarGoogle Scholar |
Bunce JA
(2005) Seed yield of soybeans with daytime or continuous elevation of carbon dioxide under field conditions. Photosynthetica 43, 435–438.
| Crossref | GoogleScholarGoogle Scholar |
Clarke PJ, Davison EA
(2004) Emergence and survival of herbaceous seedlings in temperate grassy woodlands: recruitment limitations and regeneration niche. Austral Ecology 29, 320–331.
| Crossref | GoogleScholarGoogle Scholar |
Conroy JP,
Milham PJ, Barlow E
(1992) Effect of nitrogen and phosphorus availability on the growth response of Eucalyptus grandis to high CO2. Plant, Cell & Environment 15, 843–847.
| Crossref | GoogleScholarGoogle Scholar |
Conroy JP,
Seneweera SP,
Basra AS,
Rogers GS, Nissen-Wooler B
(1994) Influence of rising atmospheric CO2 concentration and temperature on growth, yield and grain quality of cereal crops. Australian Journal of Botany 21, 741–758.
Cotching WE,
Cooper J,
Sparrow LA,
McCorkell BE,
Rowley W, Hawkins K
(2002) Effects of agricultural management on vertosols in Tasmania. Australian Journal of Soil Research 40, 1267–1286.
| Crossref | GoogleScholarGoogle Scholar |
Davey PA,
Olcer H,
Zakhleniuk O,
Bernacchi CJ,
Calfapietra C,
Long SP, Raines CA
(2006) Can fast-growing plantation trees escape biochemical down-regulation of photosynthesis when grown throughout their complete production cycle in the open air under elevated carbon dioxide? Plant, Cell & Environment 29, 1235–1244.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Day RW, Quinn GP
(1989) Comparisons of treatments after an analysis of variance in ecology. Ecological Monographs 59, 433–463.
| Crossref | GoogleScholarGoogle Scholar |
De Valpine P, Harte J
(2001) Plant responses to experimental warming in a montane meadow. Ecology 82, 637–648.
Dippery JKT,
Tissue DT,
Thomas RB, Strain BR
(1995) Effects of low and elevated CO2 and C3 and C4 annuals. I. Growth and biomass allocation. Oecologia 101, 13–20.
| Crossref | GoogleScholarGoogle Scholar |
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 |
Dunne JA,
Saleska SR,
Fischer ML, Harte J
(2004) Integrating experimental and gradient methods in ecological climate change research. Ecology 85, 904–916.
| Crossref | GoogleScholarGoogle Scholar |
Edwards GR, Crawley MJ
(1999) Herbivores, seed banks and seedling recruitment in mesic grassland. Journal of Ecology 87, 423–435.
| Crossref | GoogleScholarGoogle Scholar |
Edwards GR,
Clark H, Newton PCD
(2001a) The effects of elevated CO2 on seed production and seedling recruitment in a sheep-grazed pasture. Oecologia 127, 383–394.
| Crossref | GoogleScholarGoogle Scholar |
Edwards GR,
Newton PCD,
Tilbrook JC, Clark H
(2001b) Seedling performance of pasture species under elevated CO2. New Phytologist 150, 359–369.
| Crossref | GoogleScholarGoogle Scholar |
Edwards GR,
Hay MJM, Brock JL
(2005) Seedling recruitment dynamics of forage and weed species under continuous and rotational sheep grazing in a temperate New Zealand pasture. Grass and Forage Science 60, 186–199.
| Crossref | GoogleScholarGoogle Scholar |
Garbutt K, Bazzaz F
(1984) The effects of elevated CO2 on plants. III. Flower, fruit and seed production and abortion. New Phytologist 98, 433–446.
| Crossref | GoogleScholarGoogle Scholar |
Gloser J, Barták M
(1994) Net photosynthesis, growth rate and biomass allocation in a rhizomatous grass Calamagrostis epigejos grown at elevated CO2 concentration. Photosynthetica 30, 145–150.
Gorissen A,
Tietema A,
Joosten NN,
Estiarte M,
Penuelas J,
Sowerby A,
Emmett BA, Beier C
(2004) Climate change affects carbon allocation to the soil in shrublands. Ecosystems 7, 650–661.
| Crossref |
Grime JP,
Brown VK,
Thompson K,
Masters GJ,
Hillier SH,
Clarke IP,
Askew AP,
Corker D, Kielty JP
(2000) The response of two contrasting limestone grasslands to simulated climate change. Science 289, 762–765.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Gugerli F, Bauert MR
(2001) Growth and reproduction of Polygonum viviparum show weak responses to experimentally increased temperature at a Swiss Alpine site. Botanica Helvetica 111, 169–180.
Hattenschwiler S, Zumbrunn T
(2006) Hemiparasite abundance in an alpine treeline ecotone increases in response to atmospheric CO2 enrichment. Oecologia 147, 47–52.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hattersley P
(1983) The distribution of C3 and C4 grasses in Australia in relation to climate. Oecologia 57, 113–128.
| Crossref | GoogleScholarGoogle Scholar |
He JS,
Wolfe-Bellin KS, Bazzaz FA
(2005) Leaf-level physiology, biomass, and reproduction of Phytolacca americana under conditions of elevated CO2 and altered temperature regimes. International Journal of Plant Sciences 166, 615–622.
| Crossref | GoogleScholarGoogle Scholar |
Hendrey GR,
Lewin KF, Nagy J
(1993) Free air carbon dioxide enrichment: development, progress, results. Vegetatio 104–105, 17–31.
| Crossref | GoogleScholarGoogle Scholar |
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 |
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 | PubMed |
Hovenden MJ, Morris DI
(2002) Occurrence and distribution of native and introduced C-4 grasses in Tasmania. Australian Journal of Botany 50, 667–675.
| Crossref | GoogleScholarGoogle Scholar |
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 |
Hungate BA,
Stiling P,
Dijkstra P,
Johnson DW,
Ketterer G,
Hymus G,
Hinkle CR, Drake BG
(2004) CO2 elicits long-term decline in nitrogen fixation. Science 304, 1291.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hymus GJ,
Pontailler JY,
Li J,
Stiling P,
Hinkle CR, Drake BG
(2002) Seasonal variability in the effect of elevated CO2 on ecosystem leaf area index in a scruboak ecosystem. Global Change Biology 8, 931–940.
| Crossref | GoogleScholarGoogle Scholar |
Jablonski L,
Wang X, Curtis P
(2002) Plant reproduction under elevated CO2 conditions: a meta-analysis of reports on 79 crop and wild species. New Phytologist 156, 9–26.
| Crossref | GoogleScholarGoogle Scholar |
Kimball BA
(1983) Carbon dioxide and agricultural yield: an assemblage and analysis of 430 prior observations. Agronomy Journal 75, 779–788.
Körner C
(2003) Nutrients and sink activity drive plant CO2 responses—caution with literature-based analysis. New Phytologist 159, 537–538.
| Crossref | GoogleScholarGoogle Scholar |
Long SP,
Ainsworth EA,
Rogers A, Ort DR
(2004) Rising atmospheric carbon dioxide: plants FACE the future. Annual Review of Plant Biology 55, 591–628.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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 |
Moran MD
(2003) Arguments for rejecting the sequential Bonferroni in ecological studies. Oikos 100, 403–405.
| Crossref | GoogleScholarGoogle Scholar |
Morgan JA,
Mosier AR,
Milchunas DG,
LeCain DR,
Nelson JA, Parton WJ
(2004) CO2 enhances productivity, alters species composition, and reduces digestibility of shortgrass steppe vegetation. Ecological Applications 14, 208–219.
| Crossref | GoogleScholarGoogle Scholar |
Morgan JW
(2001) Seedling recruitment patterns over 4 years in an Australian perennial grassland community with different fire histories. Journal of Ecology 89, 908–919.
| Crossref | GoogleScholarGoogle Scholar |
Navas M,
Sonie L,
Richarte J, Roy J
(1997) The influence of elevated CO2 on species phenology, growth and reproduction in a Mediterranean old-field community. Global Change Biology 3, 523–530.
| Crossref | GoogleScholarGoogle Scholar |
Newton PCD
(1991) Direct effects of increasing carbon dioxide on pasture plants and communities. New Zealand Journal of Agricultural Research 34, 1–24.
Ofir M, Kigel J
(2003) Variation in onset of summer dormancy and flowering capacity along an aridity gradient in Poa bulbosa L., a geophytic perennial grass. Annals of Botany 91, 391–400.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Overdieck D
(1986) Long-term effects of an increased CO2 concentration on terrestrial plants in model ecosystems. Morphology and reproduction of Trifolium repens L. & Lolium perenne L. International Journal of Biometeorology 30, 323–332.
| Crossref | GoogleScholarGoogle Scholar |
Owensby CE,
Ham JM,
Knapp AK, Auen LM
(1999) Biomass production and species composition change in a tallgrass prairie ecosystem after long-term exposure to elevated atmospheric CO2. Global Change Biology 5, 497–506.
| Crossref | GoogleScholarGoogle Scholar |
Penuelas J, Filella I
(2001) Phenology—responses to a warming world. Science 294, 793–795.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Perneger TV
(1998) What’s wrong with Bonferroni adjustments. BMJ 316, 1236–1238.
| PubMed |
Poorter H, Navas ML
(2003) Plant growth and competition at elevated CO2: on winners, losers and functional groups. New Phytologist 157, 175–198.
| Crossref | GoogleScholarGoogle Scholar |
Poorter H, Perez Soba M
(2001) The growth response of plants to elevated CO2 under non-optimal environmental conditions. Oecologia 129, 1–20.
| Crossref | GoogleScholarGoogle Scholar |
Potvin C, Vasseur L
(1997) Long-term CO2 enrichment of a pasture community: species richness, dominance, and succession. Ecology 78, 666–677.
Reich PB,
Tilman D,
Craine J,
Ellsworth D,
Tjoelker MG,
Knops J,
Wedin D,
Naeem S,
Bahauddin D,
Goth J,
Bengtson 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 |
Rogers A,
Gibon Y,
Stitt M,
Morgan PB,
Bernacchi CJ,
Ort DR, Long SP
(2006) Increased C availability at elevated carbon dioxide concentration improves N assimilation in a legume. Plant, Cell & Environment 29, 1651–1658.
| Crossref | GoogleScholarGoogle Scholar |
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 |
Shaw MR,
Zavaleta ES, Chiariello NR
(2002) Grassland responses to global environmental changes suppressed by elevated CO2. Science 298, 1987–1990.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Stampfli A, Zeiter M
(2004) Plant regeneration directs changes in grassland composition after extreme drought: a 13-year study in southern Switzerland. Journal of Ecology 92, 568–576.
| Crossref | GoogleScholarGoogle Scholar |
Sternberg M,
Brown VK,
Masters GJ, Clarke IP
(1999) Plant community dynamics in a calcareous grassland under climate change manipulations. Plant Ecology 143, 29–37.
| Crossref | GoogleScholarGoogle Scholar |
Stevens MHH,
Bunker DE,
Schnitzer SA, Carson WP
(2004) Establishment limitation reduces species recruitment and species richness as soil resources rise. Journal of Ecology 92, 339–347.
| Crossref | GoogleScholarGoogle Scholar |
Stöcklin J, Körner C
(1999) Interactive effects of CO2, P availability and legume presence on calcareous grassland: results of a glasshouse experiment. Functional Ecology 13, 200–209.
| Crossref | GoogleScholarGoogle Scholar |
Thurig B,
Korner C, Stocklin J
(2003) Seed production and seed quality in a calcareous grassland in elevated CO2. Global Change Biology 9, 873–884.
| Crossref | GoogleScholarGoogle Scholar |
Tilman D
(1997) Community invasibility, recruitment limitation, and grassland biodiversity. Ecology 78, 81–92.
Totland O, Alatalo JM
(2002) Effects of temperature and date of snowmelt on growth, reproduction, and flowering phenology in the arctic/alpine herb, Ranunculus glacialis. Oecologia 133, 168–175.
| Crossref | GoogleScholarGoogle Scholar |
Verhoeven KJF,
Simonsen KL, Mcintyre LM
(2005) Implementing false discovery rate control: increasing your power. Oikos 108, 643–647.
| Crossref | GoogleScholarGoogle Scholar |
Wan SQ,
Hui DF,
Wallace L, Luo YQ
(2005) Direct and indirect effects of experimental warming on ecosystem carbon processes in a tallgrass prairie. Global Biogeochemical Cycles 19,
| Crossref |
Wand S,
Midgley G,
Jones M, Curtis P
(1999a) Responses of wild C4 and C3 grass (Poaceae) species to elevated atmospheric CO2 concentration: a meta-analytic test of current theories and perceptions. Global Change Biology 5, 723–741.
| Crossref | GoogleScholarGoogle Scholar |
Wand SJE,
Midgley GF,
Jones MH, Curtis PS
(1999b) Responses of wild C4 and C3 grass (Poaceae) species to elevated atmospheric CO2 concentration: a meta-analytic test of current theories and perceptions. Global Change Biology 5, 723–741.
| Crossref | GoogleScholarGoogle Scholar |
Winkler JB, Herbst M
(2004) Do plants of a semi-natural grassland community benefit from long-term CO2 enrichment? Basic and Applied Ecology 5, 131–143.
| Crossref | GoogleScholarGoogle Scholar |
Woodward FI, Lomas MR
(2004) Vegetation dynamics—simulating responses to climatic change. Biological Reviews 79, 643–670.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Zanetti S,
Hartwig UA,
van Kessel C,
Lüscher A,
Hebeisen T,
Frehner M,
Fischer BU,
Blum HH, Nösberger J
(1997) Does nitrogen nutrition restrict the CO2 response of fertile grassland lacking legumes? Oecologia 112, 17–25.
| Crossref | GoogleScholarGoogle Scholar |
Zangerl DD, Bazzaz FA
(1984) The response of plants to elevated CO2. II. Competitive interactions among annual plants under varying light and nutrients. Oecologia 62, 412–417.
| Crossref | GoogleScholarGoogle Scholar |
Zavaleta ES,
Shaw MR,
Chiariello NR,
Mooney HA, Field CB
(2003a) Additive effects of simulated climate changes, elevated CO2, and nitrogen deposition on grassland diversity. Proceedings of the National Academy of Sciences, USA 100, 7650–7654.
| Crossref | GoogleScholarGoogle Scholar |
Zavaleta ES,
Shaw MR,
Chiariello NR,
Thomas BD,
Cleland EE,
Field CB, Mooney HA
(2003b) Grassland responses to three years of elevated temperature, CO2, precipitation, and N deposition. Ecological Monographs 73, 585–604.
| Crossref | GoogleScholarGoogle Scholar |