Interactive Effects of Elevated [CO2] and Soil Water Stress on Leaf Morphological and Anatomical Characteristic of Paper Birch Populations


The leaf morphological and stomatal characteristics of four paper birch (Betula papyrifera Marsh) populations, grown at four treatment conditions of carbon dioxide [CO2] and soil water levels were investigated to determine whether future increases in atmospheric [CO2] and water deficit affected the leaf characteristics. The populations from Cussion Lake, Little Oliver, Skimikin and Wayerton were grown for 12 weeks under ambient (360 ppm) and elevated (720 ppm) [CO2] at both high and low water levels. The populations significantly differed in leaf area and stomatal characteristics due to the interaction effects of [CO2], water levels and population differences. Most leaf morphological characteristics and stomatal density varied due to the effects of [CO2] and/or populations, but not due to the effect of water levels. Although elevated [CO2] alone barely affected stomatal area of the birch populations, simultaneous elevated [CO2] at both water levels had stimulated stomatal characteristics within and among the populations. Overall, elevated [CO2] reduced leaf area and increased stomatal density; and low water level resulted in smaller stomatal area, pore area and guard cell width. However, the populations responded differently to an increase in [CO2] and water levels. All populations showed plastic responses with respect to [CO2] and water levels either by decreasing stomatal area under low water level or by increasing stomatal density under elevated [CO2]. Hence, integration between and within leaf characteristics had helped paper birch populations maintain balance between [CO2] gain and water loss.

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Pyakurel, A. and Wang, J. (2014) Interactive Effects of Elevated [CO2] and Soil Water Stress on Leaf Morphological and Anatomical Characteristic of Paper Birch Populations. American Journal of Plant Sciences, 5, 691-703. doi: 10.4236/ajps.2014.55084.

Conflicts of Interest

The authors declare no conflicts of interest.


[1] Intergovernmental Panel on Climate Change-IPCC (2007) Climate Change 2007: The Physical Science Basis. In: Solomon S., Qin D. and Manning M., Eds., Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change, Cambridge University Press, Cambridge.
[2] Sitch, S., Huntingford, C., Gedney, N., Levy, P. E., Lomas, M., Piao, S.L., Betts, R., Ciais, P., Cox P., Friedlingstein, P., Jones, C.D., Prentice, I.C. and Woodward, F.I. (2008) Evaluation of the Terrestrial Carbon Cycle, Future Plant Geography and Climate-Carbon Cycle Feedbacks Using Five Dynamic Global Vegetation Models (DGVMs). Global Change Biology, 14, 2015-2039.
[3] Houghton, J.T., Ding, Y., Griggs, D.J., Noguer, M., van der Linden, P.J., Dai, X., Maskell, K. and Johnson, C.A. (2001) Climate Change 2001: The Scientific Basis. Cambridge University Press, Cambridge.
[4] Catovsky, S. and Bazzaz, F.A. (1999) Elevated CO2 Influences the Responses of Two Birch Species to Soil Moisture: Implications for Forest Community Structure. Global Change Biology, 5, 507-518.
[5] Volk, M., Niklaus, P.A. and Korner, C. (2000) Soil Moisture Effects Determine CO2 Responses of Grassland Species. Oecologia, 125, 380-388.
[6] Korner, C. (2003) Ecological Impacts of Atmospheric CO2 Enrichment on Terrestrial Ecosystems. Philosophical Transactions of the Royal Society, 361, 2023-2041.
[7] Ferris, R., Sabatti, M., Miglietta, F., Mills, R.F. and Taylor, G. (2001) Leaf Area is Stimulated in Populus by Free Air CO2 Enrichment (POPFACE), through Increased Cell Expansion and Production. Plant, Cell & Environment, 24, 305-315.
[8] Hetherington, A.M. and Woodward, F.I. (2003) The Role of Stomata in Sensing and Driving Environmental Change. Nature, 424, 901-908.
[9] Pritchard, S.G., Rogers, H.H., Prior, S.A. and Peterson, C.M. (1999) Elevated CO2 and Plant Structure: A Review. Global Change Biology, 5, 807-837. doi/10.1046/j.1365-2486.1999.00268.x
[10] McLellan, T. (2000) Geographic Variation and Plasticity of Leaf Shape and Size in Begonia dregei and B. homonyma (Begoniaceae). Botanical Journal of the Linnean Society, 132, 79-95.
[11] Heath, J. and Kerstiens, G. (1997) Effects of Elevated CO2 on Leaf Gas Exchange in Beech and Oak at Two Levels of Nutrient Supply: Consequences for Sensitivity to Drought in Beech. Plant, Cell & Environment, 20, 57-67.
[12] Kerstiens, G., Townend, J., Heath, J. and Mansfield, T.A. (1995) Effects of Water and Nutrient Availability on Physiological Responses of Woody Species to Elevated CO2. Forestry, 68, 303-315.
[13] Norby, R.J. and O’Neill, E.G. (1991) Leaf Area Compensation and Nutrient Interactions in CO2-Enriched Seedlings of Yellow-Poplar (Liriodendron tulipifera L.). New Phytologist, 117, 515-28.
[14] Meng, T.T., Ni, J. and Harrison, S.P. (2009) Plant Morphometric Traits and Climate Gradients in Northern China: A Meta-Analysis Using Quadrat and Flora Data. Annals of Botany, 104, 1217-1229.
[15] Mediavilla, S., Escudero, A. and Heilmeier, H. (2001) Internal Leaf Anatomy and Photosynthetic Resource-Use Efficiency: Interspecific and Intraspecific Comparisons. Tree Physiology, 21, 251-259.
[16] Abrams, M.D. (1999) Adaptations and Responses to Drought in Quercus Species of North America. Tree Physiology, 7, 227-238.
[17] Bruschi, P., Vendramin, G.G., Bussotti, F. and Grossoni, P. (2000) Morphological and Molecular Differentiation between Quercus petraea (Matt.) Liebl. and Quercus pubescens Wild. (Fagaceae) in Northern and Central Italy. Annals of Botany, 85, 325-333.
[18] de Lillis, M. (1991) An Ecomorphological Study of the Evergreen Leaf. Braun, Blanquetia.
[19] Norby, R.J., Wullschleger, S.D., Gunderson, C.A. and Nietch, C.T. (1995) Increased Growth Efficiency of Quercus alba Trees in a CO2-Enriched Atmosphere. New Phytologist, 131, 91-97.
[20] Sims, D.A., Seemann, J.R. and Luo, Y. (1998) Elevated CO2 Concentration Has Independent Effects on Expansion Rates and Thickness of Soybean Leaves across Light and Nitrogen Gradients. Journal of Experimental Botany, 49, 583-591.
[21] Li, W.L., Berlyn, G.P. and Ashton, P.M.S. (1996) Polyploids and Their Structural and Physiological Characteristics Relative To Water Deficit in Betula papyrifera (Betulaceae). American Journal of Botany, 83, 15-20.
[22] Pettersson, R., McDonald, A.J.S. and Stadenberg, I. (1993) Response of Small Birch Plants (Betula pendula Roth.) to Elevated CO2 and Nitrogen Supply. Plant, Cell & Environment, 16, 1115-1121.
[23] Beerling, D.J., Heath, J., Woodward, F.I. and Mansfield, T.A. (1996) Drought-CO2 Interactions in Trees: Observations and Mechanisms. New Phytologist, 134, 235-242.
[24] Woodward, F.I. and Kelly, C.K. (1995) The Influence of CO2 Concentration on Stomatal Density. New Phytologist, 131, 311-327.
[25] Lin, J., Jach, M.E. and Ceulemans, R. (2001) Stomatal Density and Needle Anatomy of Scots Pine (Pinus sylvestris) Are Affected By Elevated CO2. New Phytologist, 150, 665-674.
[26] Xiao, C.W., Sun, O.J., Zhou, G.S., Zhao, J.Z. and Wu, G. (2005) Interactive Effects of Elevated CO2 and Drought Stress on Leaf Water Potential and Growth in Caragana intermedia. Trees, 19, 712-721.
[27] Paoletti, E., Nourrisson, G., Garrec, J.P. and Raschi, A. (1998) Modifications of the Leaf Surface Structures of Quercus ilex L. in Open, Naturally CO2-Enriched Environments. Plant, Cell & Environment, 21, 1071-1075.
[28] Dancik, B.P. and Barnes, B.V. (1974) Leaf Diversity in Yellow Birch (Betula alleghaniensis). Canadian Journal of Botany, 52, 2407-2414.
[29] Pyakurel, A. and Wang, J.R. (2013) Leaf Morphological Variation among Paper Birch (Betula papyrifera Marsh.) Genotypes across Canada. Open Journal of Ecology, 3, 284-295.
[30] Senn, J., Hanhimaki, S. and Haukioja, E. (1992) Among-Tree Variation in Leaf Phenology and Morphology and Its Correlation with Insect Performance in the Mountain Birch. Oikos, 63, 215-222.
[31] Sharik, T.L. and Barnes, B.V. (1979) Natural Variation in Morphology among Diverse Populations of Yellow Birch (Betula alleghaniensis) and Sweet Birch (B. lenta). Canadian Journal of Botany, 57, 1932-1939.
[32] Safford, L., Bjorkbom, J.C. and Zasada, J.C. (1990) Betula papyrifera Marsh. Paper Birch. Forest Services, Washington DC.
[33] Tschaplinski, T.J. and Norby, R.J. (1991) Physiological Indicators of Nitrogen Response in a Short Rotation Sycamore Plantation.I.CO2 Assimilation, Photosynthetic Pigments and Soluble Carbohydrates. Physiologia Plantarum, 82, 117-126.
[34] Tschaplinski, T.J., Stewart, D.B., Hanson, P.J. and Norby, R.J. (1995) Interactions between Drought and Elevated CO2 on Growth and Gas Exchange of Seedlings of Three Deciduous Tree Species. New Phytologist, 129, 63-71.
[35] Bacelar, E.A., Correia, C.M., Moutinho-Pereira, J.M., Gonazalves, B.C., Lopes, J.I. and Torres-Pereira, J.M.G. (2004) Sclerophylly and Leaf Anatomical Traits of Five Field-Grown Olive Cultivars Growing under Drought Conditions. Tree Physiology, 24, 233-239.
[36] Xu, Z. and Zhou, G. (2008) Responses of Leaf Stomatal Density to Water Status and Its Relationship with Photosynthesis in a Grass. Journal of Experimental Botany, 59, 3317-3325.
[37] Batos, B., Vilotic, D., Orlovic, S. and Miljkovic, D. (2010) Inter and Intra-Population Variation of Leaf Stomatal Traits of Quercus robur L. in Northern Serbia. Archives of Biological Sciences, Belgrade, 62, 1125-1136.
[38] Sagaram, M., Lombardini, L. and Grauke, L.J. (2007) Variation in Leaf Anatomy of Pecan Cultivars from Three Ecogeographic Locations. Journal of American Society of Horticultural Science, 132, 592-596.
[39] Teklehaimanot, Z., Lanek, J. and Tomlinson, H.F. (1998) Provenance Variation in Morphology and Leaflet Anatomy of Parkia biglobosa and Its Relation to Drought Tolerance. Trees, 13, 96-102.
[40] Mousseau, M. and Enoch, H.Z. (1989) Carbon Dioxide Enrichment Reduces Shoot Growth in Sweet Chestnut Seedlings (Castanea sativa Mill.). Plant, Cell & Environment, 12, 927-934.
[41] Radoglou, K.M. and Jarvis, P.G. (1992) The Effects of CO2 Enrichment and Nutrient Supply on Growth Morphology and Anatomy of Phaseolus vulgaris L. Seedlings. Annals of Botany, 70, 245-256.
[42] Radoglou, K.M. and Jarvis, P.G. (1990) Effects of CO2 Enrichment on Four Poplar Clones. I. Growth and Leaf Anatomy. Annals of Botany, 65, 617-626.
[43] Gielen, B., Calfapietra, C., Sabatti, M. and Ceulemans, R. (2001) Leaf Area Dynamics in a Closed Poplar Plantation under Free-Air Carbon Dioxide Enrichment. Tree Physiology, 21, 1245-1255.
[44] Mansfield, T.A., Hetherington, A.M. and Atkinson, C.J. (1990) Some Current Aspects of Stomatal Physiology. Annual Review of Plant Physiology and Plant Molecular Biology, 41, 55-75.
[45] Woodward, F.I. (1987) Stomatal Numbers Are Sensitive to Increases in CO2 from Pre-Industrial Levels. Nature, 327, 617-618.
[46] Knapp, A.K., Cocke, M., Hamerlynck, E.P. and Owensby, C.E. (1994) Effect of Elevated CO2 on Stomatal Density and Distribution in a C4 Grass and a C3 Forb under Field Conditions. Annals of Botany, 74, 595-599.
[47] Woodward, F.I., Lake, J.A. and Quick, W.P. (2002) Stomatal Development and CO2: Ecological Consequences. New Phytologist, 153, 477-484.
[48] Banon, S., Fernandez, J.A., Franco, J.A., Torrecillas, A., Alarcon, J.J. and Sanchez-Blanco, M.J. (2004) Effects of Water Stress and Night Temperature Preconditioning on Water Relations and Morphological and Anatomical Changes of Lotus creticus Plants. Scientia Horticulturae, 101, 333-342.
[49] Pyakurel, A. and Wang, J. (Unpublished) Leaf Morphological and Stomatal Variations in Paper Birch Populations across Canada. Ph.D. Dissertation, Lakehead University, Thunder Bay.
[50] Malone, S.R., Mayeux, H.S., Johnson, H.B. and Polley, H.W. (1993) Stomatal Density and Aperture Length in Four Plant Species Grown across a Sub-Ambient CO2 Gradient. American Journal of Botany, 80, 1413-1418.
[51] Tricker, P.J., Trewin, H., Kull, O., Clarkson, G.J., Eensalu, E., Tallis, M.J., Colella, A., Doncaster, C.P., Sabatti, M. and Taylor, G. (2005) Stomatal Conductance and not Stomatal Density Determines the Long-Term Reduction in Leaf Transpiration of Poplar in Elevated CO2. Oecologia, 143, 652-660.
[52] Lake, J.A. and Woodward, F.I. (2008) Response of Stomatal Numbers to CO2 and Humidity: Control by Transpiration Rate and Abscisic Acid. New Phytologist, 179, 397-404.
[53] Richardson, A.D., Ashton, P.M.S., Berlyn, G.P., McGroddy, M.E. and Cameron, I.R. (2001) Within-Crown Foliar Plasticity of Western Hemlock, Tsuga heterophylla, in Relation to Stand Age. Annals of Botany, 88, 1007-1015.
[54] Sekiya, N. and Yano, K. (2008) Stomatal Density of Cowpea Correlates with Carbon Isotope Discrimination in Different Phosphorus, Water and CO2 Environments. New Phytologist, 179, 799-807.
[55] Fraser, L.H., Greenall, A., Carlyle, C., Turkington, R. and Friedman, C.R. (2009) Adaptive Phenotypic Plasticity of Pseudoroegneria spicata: Response of Stomatal Density, Leaf Area and Biomass to Changes in Water Supply and Increased Temperature. Annals of Botany, 103, 769-775.
[56] Doheny-Adams, T., Hunt, L., Franks, P.J., Beerling, D.J. and Gray, J.E. (2012) Genetic Manipulation of Stomatal Density Influences Stomatal Size, Plant Growth and Tolerance to Restricted Water Supply across a Growth Carbon Dioxide Gradient. Philosophical Transactions of the Royal Society London B: Biological Sciences, 367, 547-555.
[57] Dunlap, J.M. and Stettler, R.F. (2001) Variation in Leaf Epidermal and Stomatal Traits of Populus trichocarpa from Two Transects across the Washington Cascades. Canadian Journal of Botany, 79, 528-536.
[58] Belhadj, S., Derridj, A., Moriana, A., Gijon, M.D.C., Mevy, J.P. and Gauquelin, T. (2007) Comparative Morphology of Leaf Epidermis in Eight Populations of Atlas Pistachio (Pistacia atlantica Anacardiaceae), Microscopy Research and Technique, 70, 837-846.
[59] Camargo, M.B. and Marenco, R.A. (2011) Density, Size and Distribution of Stomata in 35 Rainforest Tree Species in Central Amazonia. Acta Amazonica, 41, 205-212.
[60] Poulos, H.M., Goodale, U.M. and Berlyn, G.P. (2007) Drought Response of Two Mexican Oak Species, Quercus laceyi and Q. sideroxyla (Fagaceae), in Relation to Elevational Position. American Journal of Botany, 94, 809-818.
[61] Dudley, S.A. (1996) Differing Selection on Plant Physiological Traits in Response to Environmental Water Availability: A Test of Adaptive Hypotheses. Evolution, 50, 92-102.

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