Differential influence of elevated CO2 on gas exchange and water use efficiency of four indigenous shrub species distributed in different sandy environments in central Inner Mongolia

  • Qiaoyan Li
  • Liming Lai
  • Jihua Zhou
  • Hui Du
  • Tianyu Guan
  • Xiaolong Zhang
  • Lianhe Jiang
  • Yuanrun Zheng
  • Yi Yu
  • Yong Gao
  • Ping An
  • Hideyuki Shimizu
Original Article
  • 15 Downloads

Abstract

In view of the increase in global warming and carbon dioxide (CO2) concentrations, it is essential to investigate the influences of climate change on plant growth and water use in arid and semi-arid grassland species. Experiments were conducted to understand the ecophysiological response of four indigenous species to elevated CO2 in the semi-arid sandy grassland of central Inner Mongolia. Seedlings of the four species were grown for 8 weeks at four different consistently elevated CO2 concentrations in the environment-controlled growth chambers. All four elevated CO2 concentrations (400, 800, 1200, 1600 ppm) were found to result in decreased stomatal conductance (26–86%), decreased transpiration rate (21–80%), increased shoot water potential (1–42%) and increased water use efficiency (WUE) (10–412%) for two Artemisia species and Caragana korshinskii. Under our experimental conditions, the two Artemisia species and C. korshinskii would benefit more than Hedysarum laeve from exposure to elevated CO2 in terms of higher shoot water potential and WUE combined with lower stomatal conductance and transpiration rate. The results indicate that in a warmer, CO2-enriched future atmospheric environment, WUE in semi-arid grasslands may be higher than previously expected. Our findings will provide information for screening appropriate species for restoration of the degraded sandy grasslands in semi-arid areas under future climate change scenarios.

Keywords

Elevated CO2 Artemisia sphaerocephala Artemisia ordosica Hedysarum laeve Caragana korshinskii 

Notes

Acknowledgements

This work was supported by the National Natural Science Foundation of China (Grant Numbers 41330749 and 41401105).

References

  1. 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 165:351–371CrossRefPubMedGoogle Scholar
  2. Ainsworth EA, Rogers A (2007) The response of photosynthesis and stomatal conductance to rising CO2: mechanisms and environmental interactions. Plant, Cell Environ 30:258–270CrossRefGoogle Scholar
  3. Amthor JS (1995) Terrestrial higher-plant response to increasing atmospheric CO2 in relation to the global carbon cycle. Glob Change Biol 1:243–274CrossRefGoogle Scholar
  4. Anderson LJ, Maherali H, Johnson HB, Polley HW, Jackson RB (2001) Gas exchange and photosynthetic acclimation over subambient to elevated CO2 in a C3–C4 grassland. Glob Change Biol 7:693–707CrossRefGoogle Scholar
  5. Barton CVM, Duursma RA, Medlyn BE, Ellsworth DS, Eamus D, Tissue DT, Adams MA, Conroy J, Crous KY, Liberloo M (2012) Effects of elevated atmospheric CO2 on instantaneous transpiration efficiency at leaf and canopy scales in Eucalyptus saligna. Glob Change Biol 18:585–595CrossRefGoogle Scholar
  6. Bauweraerts I, Wertin TM, Ameye M, Mcguire MA, Teskey RO, Steppe K (2013) The effect of heat waves, elevated CO2 and low soil water availability on northern red oak (Quercus rubra L.) seedlings. Glob Change Biol 19:517–528CrossRefGoogle Scholar
  7. Bazzaz FA, Carlson RW (1984) The response of plants to elevated CO2. I. Competition among an assemblage of annuals at two levels of soil moisture. Oecologia 62:196–198CrossRefPubMedGoogle Scholar
  8. Bell JE, Weng E, Luo Y (2015) Ecohydrological responses to multifactor global change in a tallgrass prairie: a modeling analysis. J Geophys Res Biogeosci 115:701–719Google Scholar
  9. Bernacchi CJ, VanLoocke A (2015) Terrestrial ecosystems in a changing environment: a dominant role for water. Ann Rev Plant Biol 66:599–622CrossRefGoogle Scholar
  10. Boeck HJD, Lemmens CMHM, Bossuyt H, Malchair S, Carnol M, Merckx R, Nijs I, Ceulemans R (2006) How do climate warming and plant species richness affect water use in experimental grasslands? Plant Soil 288:249–261CrossRefGoogle Scholar
  11. Boeck HJD, Lemmens CMHM, Vicca S, Berge JVD, Dongen SV, Janssens IA, Ceulemans R, Nijs I (2007) How do climate warming and species richness affect CO2 fluxes in experimental grasslands? New Phytol 175:512–522CrossRefPubMedGoogle Scholar
  12. Boeck HJD, Lemmens CMHM, Zavalloni C, Gielen B, Malchair S, Carnol M, Merckx R, Berge JVD, Ceulemans R, Nijs I (2008) Biomass production in experimental grasslands of different species richness during three years of climate warming. Biogeosci Discuss 4:585–594CrossRefGoogle Scholar
  13. Bütof A, Von Riedmatten LR, Dormann CF, Scherer-Lorenzen M, Welk E, Bruelheide H (2012) The responses of grassland plants to experimentally simulated climate change depend on land use and region. Glob Change Biol 18:127–137CrossRefGoogle Scholar
  14. Christensen L, Coughenour MB, Ellis JE, Chen ZZ (2004) Vulnerability of the Asian typical steppe to grazing and climate change. Clim Change 63:351–368CrossRefGoogle Scholar
  15. Conley MM, Kimball BA, Brooks TJ, Pinter PJ Jr, Hunsaker DJ, Wall GW, Adam NR, Lamorte RL, Matthias AD, Thompson TL (2001) CO2 enrichment increases water-use efficiency in sorghum. New Phytol 151:407–412CrossRefGoogle Scholar
  16. Cowan IR, Farquhar GD (1977) Stomatal function in relation to leaf metabolism and environment. Symp Soc Exp Biol 31:471–505PubMedGoogle Scholar
  17. Cunniff J, Jones G, Charles M, Osborne CP (2016) Yield responses of wild C3 and C4 crop progenitors to sub-ambient CO2: a test for the role of CO2 limitation in the origin of agriculture. Glob Change Biol 23:380–393CrossRefGoogle Scholar
  18. Curtis PS, Wang X (1997) A meta-analysis of elevated CO2 effects on woody plant mass, form, and physiology. Oecologia 113:299–313CrossRefGoogle Scholar
  19. Dickie JA, Parsons AJ (2012) Eco-geomorphological processes within grasslands, shrublands and badlands in the semi-arid Karoo, South Africa. Land Degrad Dev 23:534–547CrossRefGoogle Scholar
  20. Donovan LA, Ehleringer JR (1991) Ecophysiological differences among juvenile and reproductive plants of several woody species. Oecologia 86:594–597CrossRefPubMedGoogle Scholar
  21. Drake BG, Gonzalezmeler MA, Long SP (1997) More efficient plants: a consequence of rising atmospheric CO2? Ann Rev Plant Physiol Plant Mol Biol 48:609–639CrossRefGoogle Scholar
  22. Dregne HE (1991) Global status of desertification. Ann Arid Zone 30:179–185Google Scholar
  23. Eamus D (1991) The interaction of rising CO2 and temperatures with water use efficiency. Plant, Cell Environ 14:843–852CrossRefGoogle Scholar
  24. Farquhar GD, Sharkey TD (1982) Stomatal conductance and photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 33:317–345CrossRefGoogle Scholar
  25. Farrar JF, Williams ML (1991) The effects of increased atmospheric carbon dioxide and temperature on carbon partitioning, source-sink relations and respiration. Plant, Cell Environ 14:819–830CrossRefGoogle Scholar
  26. Field CB, Jackson RB, Mooney HA (1995) Stomatal responses to increased CO2: implications from the plant to the global scale. Plant, Cell Environ 18:1214–1225CrossRefGoogle Scholar
  27. Garbutt K, Williams WE, Bazzaz FA (1990) Analysis of the differential response of five annuals to elevated CO2 during growth. Ecology 71:1185–1194CrossRefGoogle Scholar
  28. Garcia RL, Long SP, Wall GW, Osborne CP, Kimball BA, Nie GY, Pinter PJ, Lamorte RL, Wechsung F (1998) Photosynthesis and conductance of spring-wheat leaves: field response to continuous free-air atmospheric CO2 enrichment. Plant, Cell Environ 21:659–669CrossRefGoogle Scholar
  29. Hu G, Liu H, Yin Y, Song Z (2016) The role of legumes in plant community succession of degraded grasslands in northern China. Land Degrad Dev 27:366–372CrossRefGoogle Scholar
  30. Hua C, Maun MA (1999) Effects of sand burial depth on seed germination and seedling emergence of Cirsium pitcheri. Plant Ecol 140:53–60CrossRefGoogle Scholar
  31. IPCC Working Group 2 (2014) Fifth assessment report. Climate change 2014: synthesis report summary for policymakersGoogle Scholar
  32. Jackson RB, Sala OE, Paruelo JM, Mooney HA (1998) Ecosystem water fluxes for two grasslands in elevated CO2. Oecologia 113:537–546CrossRefPubMedGoogle Scholar
  33. Katul G, Manzoni S, Palmroth S, Oren R (2009) A stomatal optimization theory to describe the effects of atmospheric CO2 on leaf photosynthesis and transpiration. Ann Bot 105:431–442CrossRefPubMedPubMedCentralGoogle Scholar
  34. Keenan TF, Hollinger DY, Bohrer G, Dragoni D, Munger JW, Schmid HP, Richardson AD (2013) Increase in forest water-use efficiency as atmospheric carbon dioxide concentrations rise. Nature 499:324–327CrossRefPubMedGoogle Scholar
  35. Kim SH, Sicher RC, Bae H, Gitz DC, Baker JT, Timlin DJ, Reddy VR (2006) Canopy photosynthesis, evapotranspiration, leaf nitrogen, and transcription profiles of maize in response to CO2 enrichment. Glob Change Biol 12:588–600CrossRefGoogle Scholar
  36. Knauer J, Zaehle S, Reichstein M, Medlyn BE, Forkel M, Hagemann S, Werner C (2017) The response of ecosystem water-use efficiency to rising atmospheric CO2 concentrations: sensitivity and large-scale biogeochemical implications. New Phytol 213:1654–1666CrossRefPubMedGoogle Scholar
  37. Lecain DR, Morgan JA, Mosier AR, Nelson JA (2003) Soil and plant water relations determine photosynthetic responses of C3 and C4 grasses in a semi-arid ecosystem under elevated CO2. Ann Bot 92:41–52CrossRefPubMedPubMedCentralGoogle Scholar
  38. Li F, Kang S, Zhang J (2004) Interactive effects of elevated CO2, nitrogen and drought on leaf area, stomatal conductance, and evapotranspiration of wheat. Agric Water Manag 67:221–233CrossRefGoogle Scholar
  39. Li QY, Lai LM, Du H, Cai WT, Guan TY, Zhang XL, Jiang LH, Zheng YR, Yu Y, Gao Y, An P, Shimizu H (2017) Elevated CO2 concentrations affect the growth patterns of dominant C3 and C4 shrub species differently in the Mu Us Sandy Land of Inner Mongolia. Botany 95:869–887CrossRefGoogle Scholar
  40. Liu F, Andersen MN, Jacobsen SE, Jensen CR (2005) Stomatal control and water use efficiency of soybean (Glycine max L. Merr.) during progressive soil drying. Environ Exp Bot 54:33–40CrossRefGoogle Scholar
  41. Machado S, Paulsen GM (2001) Combined effects of drought and high temperature on water relations of wheat and sorghum. Plant Soil 233:179–187CrossRefGoogle Scholar
  42. Medlyn BE, Cvm B, Msj B, Ceulemans R, De AP, Forstreuter M, Freeman M, Jackson SB, Kellomaki S, Laitat E (2001) Stomatal conductance of forest species after long-term exposure to elevated CO2 concentration: a synthesis. New Phytol 149:247–264CrossRefGoogle Scholar
  43. Miao SL, Wayne PM, Bazzaz FA (1992) Elevated CO2 differentially alters the responses of co-occurring birch and maple seedlings to a moisture gradient. Oecologia 90:300–304CrossRefPubMedGoogle Scholar
  44. Milcu A, Lukac M, Subke JA (2012) Biotic carbon feedbacks in a materially closed soil–vegetation–atmosphere system. Nat Clim Change 2:291–294CrossRefGoogle Scholar
  45. Morgan JA, LeCain DR, Mosier AR, Milchunas DG (2001) Elevated CO2 enhances water relations and productivity and affects gas exchange in C3 and C4 grasses of the Colorado shortgrass steppe. Glob Change Biol 7:451–466CrossRefGoogle Scholar
  46. Morgan JA, Pataki DE, Körner C, Clark H, Grosso SJD, Grünzweig JM, Knapp AK, Mosier AR, Newton PCD, Niklaus PA (2004) Water relations in grassland and desert ecosystems exposed to elevated atmospheric CO2. Oecologia 1:11–25CrossRefGoogle Scholar
  47. Morgan JA, Milchunas DG, Lecain DR, West M, Mosier AR (2007) Carbon dioxide enrichment alters plant community structure and accelerates shrub growth in the shortgrass steppe. Proc Nati Acad Sci USA 104:14724–14729CrossRefGoogle Scholar
  48. Morgan JA, Lecain DR, Pendall E, Blumenthal DM, Kimball BA, Carrillo Y, Williams DG, Heisler-White J, Dijkstra FA, West M (2011) C4 grasses prosper as carbon dioxide eliminates desiccation in warmed semi-arid grassland. Nature 476:202–205CrossRefPubMedGoogle Scholar
  49. Mukhopadhyay S, Maiti SK (2014) Soil CO2 flux in grassland, afforested land and reclaimed coalmine overburden dumps: a case study. Land Degrad Dev 25:216–227CrossRefGoogle Scholar
  50. Nelson JA, Morgan JA, LeCain DR, Mosier A, Milchunas DG, Parton BA (2004) Elevated CO2 increases soil moisture and enhances plant water relations in a long-term field study in semi-arid shortgrass steppe of Colorado. Plant Soil 259:169–179CrossRefGoogle Scholar
  51. Nie D, He H, Mo G, Kirkham MB, Kanemasu ET (1992) Canopy photosynthesis and evapotranspiration of rangeland plants under doubled carbon-dioxide in closed-top chambers. Agric For Meteorol 61:205–217CrossRefGoogle Scholar
  52. Niu S, Xing X, Zhang Z, Xia J, Zhou X, Song B, Li L, Wan S (2011) Water-use efficiency in response to climate change: from leaf to ecosystem in a temperate steppe. Glob Change Biol 17:1073–1082CrossRefGoogle Scholar
  53. Norby RJ, Luo YQ (2004) Evaluating ecosystem responses to rising atmospheric CO2 and global warming in a multi-factor world. New Phytol 162:281–293CrossRefGoogle Scholar
  54. Nowak RS, Ellsworth DS, Smith SD (2004) Functional responses of plants to elevated atmospheric CO2—do photosynthetic and productivity data from FACE experiments support early predictions? New Phytol 162:253–280CrossRefGoogle Scholar
  55. Oren R, Waring RH, Stafford SG, Barrett JW (1987) Twenty-four years of ponderosa pine growth in relation to canopy leaf area and understory competition. For Sci 33:538–547Google Scholar
  56. Parentm B, Turc O, Gibon Y, Stitt M, Tardieu F (2010) Modelling temperature-compensated physiological rates, based on the co-ordination of responses to temperature of developmental processes. J Exp Bot 61:2057–2069CrossRefGoogle Scholar
  57. Patterson DT, Flint EP (1991) Impact of carbon dioxide, trace gases, and climate change on global agriculture. American Society of Agronomy, LondonGoogle Scholar
  58. 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 361:61–64CrossRefGoogle Scholar
  59. Qi J (1998) Aerial sowing for sand control in China. Science Press, BeijingGoogle Scholar
  60. Qiao YZ (2010) Effects of elevated CO2 concentration on growth and water use efficiency of winter wheat under two soil water regimes. Agric Water Manag 97:1742–1748CrossRefGoogle Scholar
  61. Rozema J, Dorel F, Janissen R, Lenssen G, Broekman R, Arp W, Drake BG (1991) Effect of elevated atmospheric CO2 on growth, photosynthesis and water relations of salt marsh grass species. Aquat Bot 39:45–55CrossRefGoogle Scholar
  62. Sage RF, Kubien DS (2007) The temperature response of C3 and C4 photosynthesis. Plant, Cell Environ 30:1086–1106CrossRefGoogle Scholar
  63. Saleska SR, Harte J, Torn MS (1999) The effect of experimental ecosystem warming on CO2 fluxes in a montane meadow. Glob Change Biol 5:125–141CrossRefGoogle Scholar
  64. Schulze ED, Robichaux RH, Grace J, Rundel PW, Ehleringer JR (1987) Plant water balance. Bioscience 37:30–37CrossRefGoogle Scholar
  65. Sellers PJ, Bounoua L, Collatz GJ, Randall DA, Dazlich DA, Los SO, Berry JA, Fung I, Tucker CJ, Field CB (1996) Comparison of radiative and physiological effects of doubled atmospheric CO2 on climate. Science 271:1402–1406CrossRefGoogle Scholar
  66. Shaw MR, Zavaleta ES, Chiariello NR, Cleland EE, Mooney HA, Field CB (2002) Grassland responses to global environmental changes suppressed by elevated CO2. Science 298:1987–1990CrossRefPubMedGoogle Scholar
  67. Sje W, Ps JMC, Midgley GF (1999) Responses of wild C4 and C3 grass (Poaceae) species to elevated atmospheric CO2 concentration: a meta-analytic test of current theories and perceptions. Glob Change Biol 5:723–741 (Review) CrossRefGoogle Scholar
  68. Smith SD, Huxman TE, Zitzer SF, Charlet TN, Housman DC, Coleman JS, Fenstermaker LK, Seemann JR, Nowak RS (2000) Elevated CO2 increases productivity and invasive species success in an arid ecosystem. Nature 408:79–82CrossRefPubMedGoogle Scholar
  69. Stitt M (1991) Rising CO2 levels and their potential significance for carbon flow in photosynthetic cells. Plant, Cell Environ 14:741–762CrossRefGoogle Scholar
  70. Strain BR (1987) Direct effects of increasing atmospheric CO2 on plants and ecosystems. Trends Ecol Evol 2:18–21CrossRefPubMedGoogle Scholar
  71. Thomas JF, Harvey CN (1983) Leaf anatomy of four species grown under continuous CO2 enrichment. Bot Gaz 144:303–309CrossRefGoogle Scholar
  72. Thomey ML, Collins SL, Vargas R, Johnson JE, Brown RF, Natvig DO, Friggens MT (2011) Effect of precipitation variability on net primary production and soil respiration in a Chihuahuan Desert grassland. Glob Change Biol 17:1505–1515CrossRefGoogle Scholar
  73. Volk M, Niklaus PA, Körner C (2000) Soil moisture effects determine CO2 responses of grassland species. Oecologia 125:380–388CrossRefPubMedGoogle Scholar
  74. Wang KY, Kellomäki S (1997) Stomatal conductance and transpiration in shoots of Scots pine after 4-year exposure to elevated CO2 and temperature. Can J Bot 75:552–561CrossRefGoogle Scholar
  75. Ward JK, Strain BR (1999) Elevated CO2 studies: past, present and future. Tree Physiol 19:211–220CrossRefPubMedGoogle Scholar
  76. Woodward FI (1990) Global change: translating plant ecophysiological responses to ecosystems. Trends Ecol Evol 5:308–311CrossRefPubMedGoogle Scholar
  77. Wu B, Ci LJ (2002) Landscape change and desertification development in the Mu Us Sandland, northern China. J Arid Environ 50:429–444CrossRefGoogle Scholar
  78. Wullschleger SD, Tschaplinski TJ, Norby RJ (2002) Plant water relations at elevated CO2 implications for water-limited environments. Plant, Cell Environ 25:319–331CrossRefGoogle Scholar
  79. Xu LK (2004) Predicted versus measured photosynthetic water-use efficiency of crop stands under dynamically changing field environments. J Exp Bot 55:2395–2411CrossRefPubMedGoogle Scholar
  80. Xu Z, Shimizu H, Ito S, Yagasaki Y, Zou C, Zhou G, Zheng Y (2014) Effects of elevated CO2, warming and precipitation change on plant growth, photosynthesis and peroxidation in dominant species from north China grassland. Planta 239:421–435CrossRefPubMedGoogle Scholar
  81. Xu Z, Jiang Y, Zhou G (2015) Response and adaptation of photosynthesis, respiration, and antioxidant systems to elevated CO2 with environmental stress in plants. Front Plant Sci 6:701PubMedPubMedCentralGoogle Scholar
  82. Yang H, Zhang J, Li Z, Wu B, Zhang Z, Wang Y (2008) Comparative study on spatial patterns of the Artemisia ordosica population in the Mu Us sandy land. Acta Ecol Sin 28:1901–1910CrossRefGoogle Scholar
  83. Zhang X (1994) Principles and optimal models for development of Maowusu Sandy grassland. Acta Phytoecol Sin 18:1–16Google Scholar
  84. Zheng YR, Xie ZX, Rimmington GM, Yu Y, Gao Y, Zhou GSH, An P, Li X, Tsuji W, Shimizu H (2010) Elevated CO2 accelerates net assimilation rate and enhance growth of dominant shrub species in a sand dune in central Inner Mongolia. Environ Exp Bot 68:31–36CrossRefGoogle Scholar
  85. Zhu Q, Jiang H, Peng CH, Liu J, Wei XH, Fang X, Liu S, Zhou GM, Yu SQ (2011) Evaluating the effects of future climate change and elevated CO2 on the water use efficiency in terrestrial ecosystems of China. Ecol Model 222:2414–2429CrossRefGoogle Scholar

Copyright information

© The Ecological Society of Japan 2018

Authors and Affiliations

  • Qiaoyan Li
    • 1
    • 2
  • Liming Lai
    • 1
  • Jihua Zhou
    • 1
  • Hui Du
    • 1
  • Tianyu Guan
    • 1
    • 2
  • Xiaolong Zhang
    • 1
    • 2
  • Lianhe Jiang
    • 1
  • Yuanrun Zheng
    • 1
  • Yi Yu
    • 3
  • Yong Gao
    • 4
  • Ping An
    • 5
  • Hideyuki Shimizu
    • 3
  1. 1.Key Laboratory of Plant Resources, West China Subalpine Botanical GardenInstitute of Botany, Chinese Academy of SciencesBeijingChina
  2. 2.University of Chinese Academy of SciencesBeijingChina
  3. 3.National Institute for Environmental StudiesTsukubaJapan
  4. 4.Inner Mongolia Agricultural UniversityHohhotChina
  5. 5.Arid Land Research CenterTottori UniversityTottoriJapan

Personalised recommendations