Abstract
Plant responses to carbon (C) and water availability are strongly connected. Thus, we can learn much about the responses of modern plants to rising atmospheric carbon dioxide (CO2) by studying their performance under a range of carbon and water availabilities, including very low CO2 as in past glacial periods. We hypothesized that, especially in shallow soils, the positive effects of high CO2 and the negative effects of low CO2 on growth response to drought are moderated by plant size-driven feedbacks through transpiration and soil water depletion. We grew two temperate annual C3 species, Avena sativa and Chenopodium album, in glacial (180 ppm), modern (400 ppm) and future (700 ppm) CO2 levels and five soil water regimes in climate chambers. In both species, low CO2 resulted in a much lower relative growth rate, biomass and total leaf area than at ambient CO2 with higher water availability, but this difference disappeared steadily towards severe drought conditions. Elevated CO2 increased relative growth rate, plant biomass and total leaf area of both species slightly compared with ambient CO2. These results were especially pronounced under drought. Our results support the hypothesis that, in annuals, plant size modulates the negative drought effect at low CO2. However, plant size-mediated effects of high CO2 on growth response to drought were inconclusive. Further experiments should reveal the interactive effects of CO2 and water regimes in environments closer to a field setting, both in shallow and in deep soils with unconstrained rooting, as well as in mixed communities.
Similar content being viewed by others
References
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 properties and plant production to rising CO2. New Phytol 165:351–372
Arp WJ (1991) Effects of source-sink relations on photosynthetic acclimation to elevated CO2. Plant Cell Environ 14:869–875
Asshoff R, Zotz G, Körner C (2006) Growth and phenology of mature temperate forest trees in elevated CO2. Global Change Biol 12:848–861
Becklin KM, Medeiros JS, Sale KR, Ward JK (2014) Evolutionary history underlies plant physiological responses to global change since the last glacial maximum. Ecol Lett 17:691–699
Beerling DJ, Chaloner WG (1993) Evolutionary responses of stomatal density to global CO2 change. Biol J Linn Soc 48:343–353
Beerling DJ, Royer DL (2002) Reading a CO2 signal from fossil stomata. New Phytol 153:387–397
Beerling DJ, Taylor LL, Bradshaw CDC, Lunt DJ, Valdes PJ, Banwart SA, Pagani M, Leake JR (2012) Ecosystem CO2 starvation and terrestrial silicate weathering: mechanisms and global-scale quantification during the late Miocene. J Ecol 100:31–41
Bettarini I, Vaccari FP, Miglietta F (1998) Elevated CO2 concentrations and stomatal density: observations from 17 plant species growing in a CO2 spring in central Italy. Global Change Biol 4:17–22
Bosabalidis A, Kofidis G (2002) Comparative effects of drought stress on leaf anatomy of two olive cultivars. Plant Sci 163:375–379
Brodribb TJ, McAdam SAM, Jordan GJ, Field TS (2009) Evolution of stomatal responsiveness to CO2 and optimization of water-use efficiency among land plants. New Phytol 183:839–847
Campbell CD, Sage RF (2006) Interactions between the effects of atmospheric CO2 content and P nutrition on photosynthesis in white lupin (Lupinus albus L.). Plant Cell Environ 29:844–853
Casper BB, Forseth IN, Wait DA (2005) Variation in carbon isotope discrimination in relation to plant performance in a natural population of Cryptantha flava. Oecologia 145:541–548
Coleman JS, McConnaughay KDM, Bazzaz FA (1993) Elevated CO2 and plant nitrogen-use: is reduced tissue nitrogen concentration size-dependent? Oecologia 93:195–200
Coley PD, Massa M, Lovelock CE, Winter K (2002) Effects of elevated CO2 on foliar chemistry of saplings of nine species of tropical tree. Oecologia 133:62–69
Cotrufo MF, Ineson P, Scott A (1998) Elevated CO2 reduces the nitrogen concentration of plant tissures. Global Change Biol 4:43–54
Dippery JK, Tissue DT, Thomas RB, Strain BR (1995) Effects of low and elevated CO2 on C3 and C4 annuals I. Growth and biomass allocation. Oecologia 101:13–20
Ehleringer JR, Cerling TE, Helliker BR (1997) C4 photosynthesis, atmospheric CO2, and climate. Oecologia 112:285–299
Fleisher DH, Timlin DJ, Reddy VR (2008) Elevated carbon dioxide and water stress effects on potato canopy gas exchange, water use, and productivity. Agric Forest Meteorol 148:1109–1122
Franks PJ, Adams MA, Amthor JS, Barbour MM, Berry JA, Ellsworth DS, Farquhar GD, Ghannoum O, Lloyd J, McDowell N, Norby RJ, Tissue DT, von Caemmerer S (2013) Sensitivity of plants to changing atmospheric CO2 concentration: from the geological past to the next century. New Phytol 197:1077–1094
Freschet GT, Cornelissen JHC, Van Logtestijn RSP, Aerts R (2010) Evidence of the ‘plant economics spectrum’ in a subarctic flora. J Ecol 98:362–373
Freschet GT, Swart E, Cornelissen JHC (2015) Integrated plant phenotypic responses to contrasting above and belowground resources: key roles of specific leaf area and root mass fraction. New Phytol 206:1247–1260
Gerhart LM, Ward JK (2010) Plant responses to low CO2 of the past. New Phytol 188:674–695
Ghannoum O, Phillips NG, Conroy JP, Smith RA, Attard RD, Woodfield R et al (2010) Exposure to preindustrial, current and future atmospheric CO2 and temperature differentially affects growth and photosynthesis in Eucalyptus. Global Change Biol 16:303–319
Gill RA, Polley HW, Johnson HB, Anderson LJ, Maherali H, Jackson RB (2002) Nonlinear grassland responses to past and future atmospheric CO2. Nature 417:279–282
Grein M, Konrad W, Wilde V, Utescher T, Roth-Nebelsick A (2011) Reconstruction of atmospheric CO2 during the early middle Eocene by application of a gas exchange model to fossil plants from the Messel Formation Germany. Palaeogeogr Palaeoclimatol Palaeoecol 309:383–391
Gulias J, Seddaiu G, Cifre J, Salis M, Ledda L (2012) Leaf and plant water use efficiency in cocksfoot and tall fescue accessions under differing soil water availability. Crop Sci 52:2321–2331
Haworth M, Elliott-Kingston C, McElwain JC (2011) The stomatal CO2 proxy does not saturate at high atmospheric CO2 concentrations: evidence from stomatal index responses of Araucariaceae conifers. Oecologia 167:11–19
Haworth M, Elliott-Kingston C, McElwain JC (2013) Co-ordination of physiological and morphological responses of stomata to elevated CO2 in vascular plants. Oecologia 171:71–82
Haworth M, Killi D, Materassi A, Raschi A (2015) Coordination of stomatal physiological behavior and morphology with carbon dioxide determines stomatal control. Am J Bot 102:677–688
Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424:901–908
Honisch B, Hemming NG, Archer D, Siddall M, McManus JF (2009) Atmospheric carbon dioxide concentration across the Mid-Pleistocene transition. Science 324:1551–1554
Huang Y, Street-Perrott FA, Metcalfe SE, Brenner M, Moreland M, Freemann KH (2001) Climate change as the dominant control on glacial-interglacial variations in C3 and C4 plant abundance. Science 293:1647–1651
IPCC (2013) Summary for policymakers. In: Stocker TF, Qin D, Plattner GK, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) Climate change 2013: the physical science basis. Contribution of Working Group I to the fifth assessment report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, New York
Kohut R (2003) The long-term effects of carbon dioxide on natural systems: issues and research needs. Environ Int 29:171–180
Kouwenberg LLR, McElwain JC, Kürschner WM, Wangner F, Beerling DJ, Mayle FE et al (2003) Stomatal frequency adjustment of four conifer species to historical changes in atmospheric CO2. Am J Bot 90:610–619
Lambers H, Poorter H (1992) Inherent variation in growth-rate between higher-plants–a search for physiological causes and ecological consequences. Adv Ecol Res 23:187–261
Lambers H, Chapin FS III, Pons TL (2008) Plant physiological ecology, 2nd edn. Springer, New York
Lambert F, Delmonte B, Petit JR, Bigler M, Kaufmann PR, Hutterli MA et al (2008) Dust-climate couplings over the past 800,000 years from the EPICA Dome C ice core. Nature 452:616–619
Leakey ADB, Lau JA (2012) Evolutionary context for understanding and manipulating plant responses to past, present and future atmospheric CO2. Philos Trans Roy Soc B 367:613–629
Lewis JD, Ward JK, Tissue DT (2010) Phosphorus supply drives nonlinear responses of cottonwood (Populus deltoides) to glacial through future CO2. New Phytol 187:438–448
Lewis JD, Simth RA, Ghannoum O, Logan BA, Phillips NG, Tissue DT (2013) Industrial-age changes in atmospheric CO2 and temperature differentially alter responses of faster- and slower-growing Eucalyptus seedlings to short-term drought. Tree Physiol 33:475–488
Lloret F, Peñuelas J, Estiarte M (2003) Ecophysiological responses of two Mediterranean shrubs, Erica multiflora and Globularia alypum, to experimentally drier and warmer conditions. Physiol Plant 119:231–243
Maherali H, DeLucia EH (2000) Interactive effects of elevated CO2 and temperature on water transport in ponderosa pine. Am J Bot 87:243–249
McElwain JC, Mayle FE, Beerling DJ (2002) Stomatal evidence for a decline in atmospheric CO2 concentration during the Younger Dryas stadial: a comparison with Antarctic ice core records. J Quat Sci 17:21–29
Medeiros JS, Ward JK (2013) Increasing atmospheric CO2 from glacial to future concentrations affects drought tolerance via impacts on leaves, xylem and their integrated function. New Phytol 199:738–748
Onoda Y, Hirose T, Hikosaka K (2009) Does leaf photosynthesis adapt to CO2-enriched environments? An experiment on plants originating from three natural CO2 springs. New Phytol 182:698–709
Perry LG, Shafroth PB, Blumenthal DM, Morgan JA, LeCain DR (2013) Elevated CO2 does not offset greater water stress predicted under climate change for native and exotic riparian plants. New Phytol 197:532–543
Picotte JJ, Rosenthal DM, Rhode JM, Cruzan MB (2007) Plastic responses to temporal variation in moisture availability: consequences for water use efficiency and plant performance. Oecologia 153:821–832
Polley HW, Johnson HB, Marino BD, Mayeux HS (1993) Increase in C3 plant water-use efficiency and biomass over glacial to present CO2 concentrations. Nature 361:61–64
Polley HW, Johnson HB, Marino BD, Mayeux HS (1994) Increasing CO2: comparative responses of the C4 grass Schizachyrium and grassland invader Prosopis. Ecology 75:976–988
Poorter H, VanBerkel Y, Baxter R, DenHertog J, Dijkstra P, Gifford RM, Griffin KL, Roumet C, Roy J, Wong SC (1997) The effect of elevated CO2 on the chemical composition and construction costs of leaves of 27 C-3 species. Plant Cell Environ 20:472–482
Poorter H, Buehler J, van Dusschoten D, Climent J, Postma JA (2012) Pot size matters: a meta-analysis of the effects of rooting volume on plant growth. Funct Plant Biol 39:839–850
Prior SA, Runion GB, Marble SC, Rogers HH, Gilliam CH, Torbert HA (2011) A review of elevated atmospheric CO2 effects on plant growth and water relations: implications for Horticulture. HortScience 46:158–162
Quirk J, McDowell NG, Leake JR, Hudson PJ, Beerling DJ (2013) Increased susceptibility to drought-induced mortality in Sequoia sempervirens (Cupressaceae) trees under Cenozoic atmospheric carbon dioxide starvation. Am J Bot 100:582–591
Royer DL (2006) CO2-forced climate thresholds during the Phanerozoic. Geochim Cosmochim Acta 70:5665–5675
Sage RF (1995) Was low atmospheric CO2 during the Pleistocene a limiting factor for the origin of agriculture? Global Change Biol 1:93–106
Sage RF, Coleman JR (2001) Effects of low atmospheric CO2 on plants: more than a thing of the past. Trends Plant Sci 6:18–24
Sinclair TR, Pinter PJ Jr, Kimball BA, Adamsen FJ, LaMorte RL, Wall GW, Hunsaker DJ, Adam N, Brooks TJ, Garcia RL, Thompson T, Leavitt S, Matthias A (2000) Leaf nitrogen concentration of wheat subjected to elevated [CO2] and either water or N deficits. Agr Ecosyst Environ 79:53–60
Stiling P, Cornelissen T (2007) How does elevated carbon dioxide (CO2) affect plant-herbivore interactions? A field experiment and meta-analysis of CO2-mediated changes on plant chemistry and herbivore performance. Global Change Biol 13:1823–1842
Temme AA, Cornwell WK, Cornelissen JHC, Aerts R (2013) Meta-analysis reveals profound responses of plant traits to glacial CO2 levels. Ecol Evol 3:4525–4535
Temme AA, Liu JC, Cornwell WK, Cornelissen JHC, Aerts R (2015) Winners always win: growth of a wide range of plant species from low to future high CO2. Ecol Evol. doi:10.1002/ece3.1687
Tissue DT, Lewis JD (2012) Learning from the past: how low CO2 studies inform plant and ecosystem response to future climate change. New Phytol 194:4–6
Tissue DT, Griffin KL, Thomas RB, Strain BR (1995) Effects of low and elevated CO2 on C3 and C4 annuals II. Photosynthesis and leaf biochemistry. Oecologia 101:21–28
Tonsor SJ, Scheiner SM (2007) Plastic trait integration across a CO2 gradient in Arabidopsis thaliana. Am Nat 169:E119–E140
Tripati AK, Roberts CD, Eagle RA (2009) Coupling of CO2 and ice sheet stability over major climate transitions of the last 20 million years. Science 326:1394–1397
Wand SJE, Midgley GF, Jones MH, Curtis PS (1999) 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 Biol 5:723–741
Ward JK, Kelly JK (2004) Scaling up evolutionary responses to elevated CO2: lessons from Arabidopsis. Ecol Lett 7:427–440
Ward JK, Tissue DT, Thomas RB, Strain BR (1999) Comparative responses of model C3 and C4 plants to drought in low and elevated CO2. Global Change Biol 5:857–867
Ward JK, Antonovics J, Thomas RB, Strain BR (2000) Is atmospheric CO2 a selective agent on model C3 annuals? Oecologia 123:330–341
Webb WL, Lauenroth WK, Szarek SR, Kinerson R (1983) Primary production and abiotic controls in forests, grasslands and desert ecosystems in the United States. Ecology 64:134–151
Weltzin JF, Bridgham SD, Pastor J, Chen JQ, Harth C (2003a) Potential effects of warming and drying on peatland plant community composition. Global Change Biol 9:141–151
Weltzin JF, Loik ME, Schwinning S, Williams DG, Fay PA, Haddad BM et al (2003b) Assessing the response of terrestrial ecosystems to potential changes in precipitation. Bioscience 53:941–952
Weyers JDB, Johansen LG (1985) Accurate estimation of stomatal aperture from silicone rubber impressions. New Phytol 101:109–115
Woodward FI (1987) Stomatal numbers are sensitive to increases in CO2 from preindustrial levels. New Phytol 69:983–992
Xu ZZ, Zhou GS (2008) Responses of leaf stomatal density to water status and its relationship with photosynthesis in a grass. J Exp Bot 59:3317–3325
Yung YL, Lee T, Wang CH, Shieh YT (1996) Dust: a diagnostic of the hydrologic cycle during the last glacial maximum. Science 27:962–963
Zeppel MJB, Lewis JD, Chaszar B, Smith RA, Medlyn BE, Huxman TE et al (2012) Nocturnal stomatal conductance responses to rising CO2, temperature and drought. New Phytol 193:929–938
Zheng SX, Shangguan (2005) Comparison of the leaf stomatal characteristic parameters of three plants in Loess Plateau over the last 70 years. J Geochem Soc Meteor Soc 14:1–5
Acknowledgments
We would like to thank our colleagues at Utrecht University, specifically R. Welschen, B. Robroeck, R. Wagner and M. Hefting, for hosting this research at the experimental CO2 manipulation facility. Feng Lin kindly provided the seeds for this study. This study was financially supported by Grant 142.16.3032 of the Darwin Center for Biogeosciences to R. Aerts; Grant CEP-12CDP007 by the Royal Netherlands Academy of Arts and Sciences to J.H.C. Cornelissen; the National Natural Science Foundation of China (31500399) and the Fundamental Research Funds for the Central Universities (XDJK2014C158) to J.C. Liu. J.C. Liu also gratefully acknowledges the Chinese Scholarship Council and the School of Life Science, SW China University for financially supporting her 1 year research visit to VU University.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
About this article
Cite this article
Liu, JC., Temme, A.A., Cornwell, W.K. et al. Does plant size affect growth responses to water availability at glacial, modern and future CO2 concentrations?. Ecol Res 31, 213–227 (2016). https://doi.org/10.1007/s11284-015-1330-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11284-015-1330-y