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 AJPS  Vol.12 No.7 , July 2021
N/P/K Ratios and CO2 Concentration Change Nitrogen-Photosynthesis Relationships in Black Spruce
Abstract: The relationship between photosynthesis and leaf nitrogen concentration is often used to model forest carbon fixation and ratios of different nutrient elements can modify this relationship. However, the effects of nutrient ratios on this important relationship are generally not well understood. To investigate whether N/P/K ratios and CO2 concentration ([CO2]) influence relationships between photosynthesis and nitrogen, we exposed one-year-old black spruce seedlings to two [CO2] (370 and 720 μmol·mol-1), two N/P/K ratio regimes (constant (CNR) and variable (VNR) nutrient ratio) at 6 N supply levels (10 to 360 μmol·mol-1). It was found that photosynthesis (Pn) was more sensitive to nitrogen supply and N/P/K ratios under the elevated [CO2] than under ambient [CO2]; under the elevated [CO2], Pn declined with increases in N supplies above 150 μmol·mol-1 in the CNR treatment but was relatively insensitive to N supplies of the same range in the VNR treatment. Further, our data suggest that the nutrient ratio and the CO2 elevation effects on photosynthesis were via their effects on the maximum rate of carboxylation (Vcmax) but not electron transport (Jmax) or triose phosphate utilization (TPU). The results suggest that the CO2 elevation increased the demand for all three nutrient elements but the increase was greater for N than for P and K. The CO2 elevation resulted in greater photosynthetic use efficiencies of N, P and K, but the increases varied with the nutrient ratio treatments. The results suggest that under elevated [CO2], higher net photosynthetic rates demand different optimal N-P-K ratios than under the current [CO2].
Cite this paper: Dang, Q. , Li, J. and Man, R. (2021) N/P/K Ratios and CO2 Concentration Change Nitrogen-Photosynthesis Relationships in Black Spruce. American Journal of Plant Sciences, 12, 1090-1105. doi: 10.4236/ajps.2021.127076.
References

[1]   Bowman, W.D. and Conant, R.T. (1994) Shoot Growth Dynamics and Photosynthetic Response to Increased Nitrogen Availability in the Alpine Willow Salix glauca. Oecologia, 97, 93-99.
https://doi.org/10.1007/BF00317912

[2]   Brady, N.C. and Weil, R.R. (2002) The Nature and Properties of Soils. Pearson Education, Upper Saddle River, 960 p.

[3]   Cao, B., Dang, Q.-L. and Zhang, S. (2007) Relationship between Photosynthesis and Leaf Nitrogen Concentration under Ambient and Elevated [CO2] in White Birch (Betula papyrifera) Seedlings. Tree Physiology, 27, 891-899.
https://doi.org/10.1093/treephys/27.6.891

[4]   Crous, K.Y., Walters, M.B. and Ellsworth, D.S. (2008) Elevated CO2 Concentration Affects Leaf Photosynthesis-Nitrogen Relationships in Pinustaeda over Nine Years in FACE. Tree Physiology, 28, 607-614.
https://doi.org/10.1093/treephys/28.4.607

[5]   Ellsworth, D.S., Reich, P.B., Naumburg, E.S., Koch, G.W., Kubiske, M.E. and Smith, S.D. (2004) Relationship between Photosynthesis and Leaf Nitrogen Concentration under Ambient and Elevated [CO2] in White Birch (Betula papyrifera) Seedlings. Global Change Biology, 10, 2121-2138.
https://doi.org/10.1111/j.1365-2486.2004.00867.x

[6]   Garnier, E., Salager, J.L., Laurent, G. and Sonie, L. (1999) Relationships between Photosynthesis, Nitrogen and Leaf Structure in 14 Grass Species and Their Dependence on the Basis of Expression. New Phytologist, 143, 119-129.
https://doi.org/10.1046/j.1469-8137.1999.00426.x

[7]   Peterson, A.G., Field, C.B., Ball, J.T., Amthor, J.S., Drake, B., Emanuel, W.R., Johnson, D.W., Hanson, P.J., Luo, Y., McMurtrie, R.E., Norby, R.J., Oechel, W.C., Clenton, E.O., Parton, W.J., Pierce, L.L., Rastetter, E.B., Ruimy, A., Running, S.W. and Zak, D.R. (1999) Reconciling the Apparent Difference between Mass- and Area-Based Expressions of the Photosynthesis-Nitrogen Relationship. Oecologia, 118, 144-150.
https://doi.org/10.1007/s004420050712

[8]   Peterson, A.G., Ball, J.T., Luo, Y., Field, C.B., Reich, P.B., Curtis, P.S., Griffin, K.L., Gunderson, C.A., Norby, R.J., Tissue, D.T., Forstreuter, M., Rey, A., Vogel, C.S., Participants, C. (1999) The Photosynthesis Leaf Nitrogen Relationship at Ambient and Elevated Atmospheric Carbon Dioxide: A Meta-Analysis. Global Change Biology, 5, 331-346.
https://doi.org/10.1046/j.1365-2486.1999.00234.x

[9]   Dewar, R.C. and McMurtrie, R.E. (1996) Analytical Model of Stemwood Growth in Relation to Nitrogen Supply. Tree Physiology, 16, 161-171.
https://doi.org/10.1093/treephys/16.1-2.161

[10]   Hirose, T. (1988) Modeling the Relative Growth-Rate as a Function of Plant Nitrogen Concentration. Physiologia Plantarum, 72, 185-189.
https://doi.org/10.1111/j.1399-3054.1988.tb06641.x

[11]   McMurtrie, R.E. (1991) Relationship of Forest Productivity to Nutrient and Carbon Supply—A Modeling Analysis. Tree Physiology, 9, 87-99.
https://doi.org/10.1093/treephys/9.1-2.87

[12]   McMurtrie, R.E., Norby, R.J., Medlyn, B.E., Dewar, R.C., Pepper, D.A., Reich, P.B. and Barton, C.V.M. (2008) Why Is Plant-Growth Response to Elevated CO2 Amplified When Water Is Limiting, but Reduced When Nitrogen Is Limiting? A Growth-Optimisation Hypothesis. Functional Plant Biology, 35, 521-534.
https://doi.org/10.1071/FP08128

[13]   Verkroost, A.W.M. and Wassen, M.J. (2005) A Simple Model for Nitrogen-Limited Plant Growth and Nitrogen Allocation. Annals of Botany, 96, 871-876.
https://doi.org/10.1093/aob/mci239

[14]   Springer, C.J., Delucia, E.H. and Thomas, R.B. (2005) Relationships between Net Photosynthesis and Foliar Nitrogen Concentrations in Loblolly Pine Forest Ecosystem Grown in Elevated Atmospheric Carbon Dioxide. Tree Physiology, 25, 385-394.
https://doi.org/10.1093/treephys/25.4.385

[15]   Kellomaki, S. and Wang, K.Y. (1997) Effects of Long-Term CO2 and Temperature Elevation on Crown Nitrigen Distribution and Daily Photosynthetic Performace of Scots Pine. Forest Ecology and Management, 99, 309-326.
https://doi.org/10.1016/S0378-1127(97)00059-5

[16]   Murthy, R., Dougherty, P.M., Zarnoch, S.J. and Allen, H.L. (1996) Effects of Carbon Dioxide, Fertilization, and Irrigation on Photosynthetic Capacity of Loblolly Pine Trees. Tree Physiology, 16, 537-546.
https://doi.org/10.1093/treephys/16.6.537

[17]   Saidana, D., Braham, M., Boujnah, D., Mariem, F.B., Ammari, S. and El Hadj, S.B. (2009) Nutrient Stress, Ecophysiological, and Metabolic Aspects of Olive Tree Cultivars. Journal of Plant Nutrition, 32, 129-145.
https://doi.org/10.1080/01904160802608999

[18]   Marschner, H. (1995) Mineral Nutrition of Higher Plants. San Academic Press, Diego, 889 p.

[19]   Nicodemus, M.A., Salifu, F.K. and Jacobs, D.F. (2008) Growth, Nutrition, and Photosynthetic Response of Black Walnut to Varying Nitrogen Sources and Rates. Journal of Plant Nutrition, 31, 1917-1936.
https://doi.org/10.1080/01904160802402856

[20]   Chapin III, F.S. (1991) Effects of Multiple Environmental Stresses on Nutrient Availability and Use. In: Mooney, H.A., Wiiner, W.E. and Pell, E.J., Eds., Response of Plants to Multiple Stresses, Academic Press, San Diego, 67-88.
https://doi.org/10.1016/B978-0-08-092483-0.50008-6

[21]   Timmer, V.R., et al. (1991) Steady-State Nutrient Preconditioning and Early Outplanting Performance of Containerized Black Spruce Seedlings. Canadian Journal of Forest Research, 21, 585-594.
https://doi.org/10.1139/x91-080

[22]   van den Driessche, R. and Ponsford, D. (1995) Nitrogen Induced Potassium Deficiency in White Spruce (Picea glauca) and Engelmann Spruce (Piceaengelmannii) Seedlings. Canadian Journal of Forest Research, 25, 1445-1454.
https://doi.org/10.1139/x95-157

[23]   Barbosa, J.G., Kampf, A.N., Martinez, H.E.P., Koller, O.C. and Bohnen, H. (2000) Chrysanthemum Cultivation in Expanded Clay. I. Effect of the Nitrogen-Phosphorus-Potassium Ratio in the Nutrient Solution. Journal of Plant Nutrition, 23, 1327-1336.
https://doi.org/10.1080/01904160009382103

[24]   Egilla, J.N. and Davies, F.T. (1995) Response of Hibiscus-rosa-sinensis L. to Varying Levels of Potassium Fertilization—Growth, Gas-Exchange and Mineral Element Concentration. Journal of Plant Nutrition, 18, 1765-1783.
https://doi.org/10.1080/01904169509365022

[25]   Campbell, C.D. and Sage, R.F. (2006) Interactions between the Effects of Atmospheric CO2 Content and P Nutrition on Photosynthesis in White Lupin (Lupinus albus L.). Plant, Cell and Environment, 29, 844-853.
https://doi.org/10.1111/j.1365-3040.2005.01464.x

[26]   Epstein, E. (1972) Mineral Nutrition of Plants: Principles and Perspectives. John Wiley and Sons, Inc., New York, 412 p.

[27]   Epstein, E. and Bloom, A.J. (2005) Mineral Nutrition of Plants: Principles and Perspectives. Sinauer Associates, Sunderland, 400 p.

[28]   Timmer, V.R. (1991) Interpretation of Seedling Analysis and Visual Symptoms. In: van den Driessche R, Editors. Mineral Nutrition of Conifer Seedlings. CRC Press, Boca Raton, 113-134.

[29]   Ingestad, T. (1979) Mineral Nitrient Requirements of Pinus silvestris and Piceaabies Seedlings. Physiol Plant, 45, 373-380.
https://doi.org/10.1111/j.1399-3054.1979.tb02599.x

[30]   Brown, K. and Higginbotham, K.O. (1986) Effects of Carbon Dioxide Enrichment and Nitrogen Supply on Growth of Boreal Tree Seedlings. Tree Physiology, 2, 223-232.
https://doi.org/10.1093/treephys/2.1-2-3.223

[31]   Griffin, K.L., Thomas, R.B. and Strain, B.R. (1993) Effects of Nitrogen Supply and Elevated Carbon Dioxide on Construction Cost in Leaves of Pinus taeda (L) Seedlings. Oecologia, 95, 575-580.
https://doi.org/10.1007/BF00317443

[32]   Gavito, M.E., Curtis, P.S., Mikkelsen, T.N. and Jakobsen, I. (2001) Interactive Effects of Soil Temperature, Atmospheric Carbon Dioxide and Soil N on Root Development, Biomass and Nutrient Uptake of Winter Wheat during Vegetative Growth. Journal of Experimental Botany, 52, 1913-1923.
https://doi.org/10.1093/jexbot/52.362.1913

[33]   Cao, B., Dang, Q.L., Yu, X. and Zhang, S. (2008) Effects of [CO2] and Nitrogen on Morphological and Biomass Traits of White Birch (Betula papyrifera) Seedlings. Forest Ecology and Management, 254, 217-224.
https://doi.org/10.1016/j.foreco.2007.08.002

[34]   Ambebe, T.F., Dang, Q.L. and Li, J. (2010) Low Soil Temperature Inhibits the Effect of High Nutrient Supply on Photosynthetic Response to Elevated Carbon Dioxide Concentration in White Birch Seedlings. Tree Physiology, 30, 234-243.
https://doi.org/10.1093/treephys/tpp109

[35]   Ripullone, F.G.G.M. and La, J.B. (2003) Photosynthesis-Nitrogen Relationships: Interpretation of Different Patterns between Pseudotruga menziesii and Populus x euroamericana in a Mini-Stand Experiment. Tree Physiology, 23, 137-144.
https://doi.org/10.1093/treephys/23.2.137

[36]   Zhang, S. and Dang, Q.L. (2006) Effects of Carbon Dioxide Concentration and Nutrition on Photosynthetic Functions of White Birch Seedlings. Tree Physiology, 26, 1457-1467.
https://doi.org/10.1093/treephys/26.11.1457

[37]   Ainsworth, E.A. and Rogers, A. (2007) The Response of Photosynthesis and Stomatal Conductance to Rising [CO2]: Mechanisms and Environmental Interactions. Plant Cell Environ, 30, 258-270.
https://doi.org/10.1111/j.1365-3040.2007.01641.x

[38]   Long, S.P., Elizabith, A.A., Rogers, A. and Ort, D.R. (2004) Rising Atmospheric Carbon Dioxide: Plants FACE the Future. Annual Review of Plant Biology, 55, 591-628.
https://doi.org/10.1146/annurev.arplant.55.031903.141610

[39]   Nowak, R.S., Ellsworth, D.S. and Smith, S.D. (2004) Functional Responses of Plants to Elevated Atmospheric CO2—Do Photosynthetic and Productivity Data from FACE Experiments Support Early Predictions? New Phytologist Foundation, 162, 253-280.
https://doi.org/10.1111/j.1469-8137.2004.01033.x

[40]   Roberntz, P. and Stockfors, J. (1998) Effects of Elevated CO2 Concentration and Nutriention on Net Photosynthesis, Stomatal Conductance and Needle Respiration of Field-Grown Norway Spruce Trees. Tree Physiology, 18, 233-241.
https://doi.org/10.1093/treephys/18.4.233

[41]   Tognetti, R. and Johnson, J.D. (1999) The Effect of Elevated Atmospheric CO2 Concentration and Nutrient Supply on Gas Exchange, Carbohydrates and Foliar Phenolic Concentration in Live Oak (Quercus virginiana Mill.) Seedlings. Annals of Forest Science, 56, 379-389.
https://doi.org/10.1051/forest:19990503

[42]   Bigras, F.J. and Bertrand, A. (2006) Responses of Piceamariana to Elevated CO2 Concentration during Growth, Cold Hardening and Dehardening: Phenology, Cold Tolerance, Photosynthesis and Growth. Tree Physiology, 26, 875-888.
https://doi.org/10.1093/treephys/26.7.875

[43]   IPCC (2007) Climate change 2007: The Physical Science Basis. Cambridge University Press, Cambridge, 996 p.

[44]   Norby, R.J. and Iversen, C.M. (2006) Nitrogen Uptake, Distribution, Turnover, and Efficiency of Use in a CO2-Enriched Sweetgum Forest. Ecology, 87, 5-14.
https://doi.org/10.1890/04-1950

[45]   Norby, R.J., Warren, J.M., Iversen, C.M., Medlyn, B.E. and McMurtrie, R.E. (2010) CO2 Enhancement of Forest Productivity Constrained by Limited Nitrogen Availability. Nature Precedings.
https://doi.org/10.1038/npre.2009.3747.1

[46]   Poorter, H. (1998) Do Slow-Growing Species and Nutrient-Stressed Plants Respond Relatively Strongly to Elevated CO2? Global Change Biology, 4, 693-697.
https://doi.org/10.1046/j.1365-2486.1998.00177.x

[47]   Rogers, A. and Ellsworth, D.S. (2002) Photosynthetic Acclimation of Pinus taeda (loblolly pine) to Long-Term Growth in Elevated pCO2 (FACE). Plant, Cell and Environment, 25, 851-858.
https://doi.org/10.1046/j.1365-3040.2002.00868.x

[48]   Davey, P.A., Olcer, H., Zakhleniuk, O., Bernacchi, C.J., Calfapietra, C., Long, S.P. and Raines, C.A. (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 and Environment, 29, 1235-1244.
https://doi.org/10.1111/j.1365-3040.2006.01503.x

[49]   Lewis, J.D., Lucash, M., Olszyk, D.M. and Tingey, D.T. (2004) Relationships between Needle Nitrogen Concentration and Photosynthetic Responses of Douglas-Fir Seedlings to Elevated CO2 and Temperature. New Phytologist, 162, 355-364.
https://doi.org/10.1111/j.1469-8137.2004.01036.x

[50]   Johnsen, K.H. (1993) Growth and Ecophysiological Responses of Black Spruce Seedlings to Elevated CO2 under Varied Water and Nutrient Additions. Canadian Journal of Forest Research, 23, 1033-1042.
https://doi.org/10.1139/x93-132

[51]   Gunderson, C.A. and Wullschleger, S.D. (1994) Photosynthetic Acclimation in Trees to Rising Atmospheric CO2: A Broader Perspective. Photosynthesis Research, 39, 369-388.
https://doi.org/10.1007/BF00014592

[52]   Kitaoa, M., Koike, T., Tobita, H. and Maruyama, Y. (2005) Elevated CO2 and Limited Nitrogen Nutrition Can Restrict Excitation Energy Dissipation in Photosystem II of Japanese White Birch (Betula platyphylla var. japonica) Leaves. Physiologia Plantarum, 125, 64-73.
https://doi.org/10.1111/j.1399-3054.2005.00540.x

[53]   Isopp, H., Frehner, M., Long, S.P. and Nosberger, J. (2000) Sucrose-Phosphate Synthase Responds Differently to Source-Sink Relations and to Photosynthetic Rates: Lolium perenne L. Growing at Elevated pCO2 in the Field. Plant, Cell and Environment, 23, 597-607.
https://doi.org/10.1046/j.1365-3040.2000.00583.x

[54]   Stitt, M. and Krapp, A. (1999) The Interaction between Elevated Carbon Dioxide and nitrogen Nutrition: The Physiological and Molecular Background. Plant, Cell and Environment, 22, 583-621.
https://doi.org/10.1046/j.1365-3040.1999.00386.x

[55]   Oren, R., Ellsworth, D.S., Johnsen, K.H., Phillips, N., Ewers, B.E., Maier, C., Schafer, K.V.R., McCarthy, H., Hendrey, G., McNulty, S.G. and Katul, G.G. (2001) Soil Fertility Limits Carbon Sequestration by Forest Ecosystems in a CO2-Enriched Atmosphere. Nature, 411, 469-472.
https://doi.org/10.1038/35078064

[56]   Saxe, H., Ellsworth, D.S. and Heath, J. (1998) Tree and Forest Functioning in an Enriched CO2 Atmosphere, Tansley Review No. 98. New Phytologist, 139, 395-436.
https://doi.org/10.1046/j.1469-8137.1998.00221.x

[57]   Zhang, S., Dang, Q.L. and Yu, X. (2006) Nutrient and [CO2] Elevation Had Synergistic Effects on Biomass Production but not on Biomass Allocation of White Birch Seedlings. Forest Ecology and Management, 234, 238-244.
https://doi.org/10.1016/j.foreco.2006.07.017

[58]   Reich, P.B., Hobbie, S.E., Lee, T., Ellsworth, D.S., West, J.B., Tilman, D., Knops, J.M.H., Naeem, S. and Trost, J. (2006) Nitrogen Limitation Constrains Sustainability of Ecosystem Response to CO2. Nature, 440, 922-925.
https://doi.org/10.1038/nature04486

[59]   Finzi, A.C., Moore, D.J.P., De Lucia, E.H., Lichter, J., Hofmockel, K.S., Jackson, R.B., Kim, H.S., Matamala, R., McCarthy, H.R., Oren, R., Pippen, J.S. and Schlesinger, W.H. (2006) Progressive Nitrogen Limitation of Ecosystem Processes under Elevated CO2 in a Warm-Temperate Forest. Ecology, 87, 15-25.
https://doi.org/10.1890/04-1748

[60]   Finzi, A.C., De Lucia, E.H., Jason, G.H,, Richter, D.D. and Schlesinger, W.H. (2002) The Nitrogen Budget of a Pine Forest under Free Air CO2 Enrichment. Oecologia, 132, 567-578.
https://doi.org/10.1007/s00442-002-0996-3

[61]   Elkohen, A. and Mousseau, M. (1994) Interactive Effects of Elevated CO2 and Mineral Nutrition on Growth and CO2 Exchange of Sweet Chestnut Seedlings (Castanea sativa). Tree Physiology, 14, 679-690.
https://doi.org/10.1093/treephys/14.7-8-9.679

[62]   Tissue, D.T. and Lewis, J.D. (2010) Photosynthetic Responses of Cottonwood Seedlings Grown in Glacial through Future Atmospheric [CO2] Vary with Phosphorus Supply. Tree Physiology, 30, 1361-1372.
https://doi.org/10.1093/treephys/tpq077

[63]   Peterson, A.G., Ball, J.T., Luo, Y., Field, C.B., Curtis, P.S., Griffin, K.L., Gunderson, C.A., Norby, R.J., Tissue, D.T., Forstreuter, M., Rey, A. and Vogel, C.S. (1999) Quantifying the Response of Photosynthesis to Changes in Leaf Nitrogen Content and Leaf Mass Per Area in Plants Grown under Atmospheric CO2 Enrichment. Plant Cell and Environment, 22, 1109-1119.
https://doi.org/10.1046/j.1365-3040.1999.00489.x

[64]   Reich, P.B., Hungate, B.A. and Luo, Y. (2006) Carbon-Nitrogen Interactions in Terrestrial Ecosystems in Response to Rising Atmospheric Carbon Dioxide. Annual Review of Ecology, Evolution, and Systematics, 37, 611-636.
https://doi.org/10.1146/annurev.ecolsys.37.091305.110039

[65]   Viereck, L.A. and Johnston, W.F. (1990) Black Spruce. In, Silvics of North America. Forest Service, Washington DC, 227-237.
https://doi.org/10.1016/S0195-5616(90)50012-1

[66]   Morrison, I.K. (1974) Mineral Nutrition of Conifers with Special Reference to Nutrient Status Interpretation: A Review of Literature. 1-74.

[67]   Landis, T.D. (1989) Mineral Nutrients and Fertilization. In: Landis, T.D., Tinus, R.W., McDonald, S.E. and Barnett, J.P., Eds., The Container Tree Nursery Manual, Department of Agriculture, Forest Service, Washington DC, 1-67.

[68]   Ingestad, T. and Agren, G.I. (1992) Theories and Methods on Plant Nutrition and Growth. Physiologia Plantarum, 84, 177-184.
https://doi.org/10.1111/j.1399-3054.1992.tb08781.x

[69]   Zhang, S.R. and Dang, Q.L. (2007) Interactive Effects of Soil Temperature and [CO2] on Morphological and Biomass Traits in Seedlings of Four Boreal Tree Species. Forest Science, 53, 453-460.

[70]   Li, J.L., Dang, Q.L., Man, R.Z. and Marfo, J. (2013) Elevated CO2 Alters N-Growth Relationship in Spruce and Causes Unequal Increases in N, P and K Demands. Forest Ecology and Management, 298, 19-26.
https://doi.org/10.1016/j.foreco.2013.02.024

[71]   Watanabe, M. et al. (2011) Growth and Photosynthetic Traits of Hybrid Larch F1 (Larix gmeliniivar. japonica × L. kaempferi) under Elevated CO2 Concentration with Low Nutrient Availability. Tree Physiology, 31, 965-975.
https://doi.org/10.1093/treephys/tpr059

[72]   Onoda, Y., Hirose, T. and Hikosaka, K. (2009) Does Leaf Photosynthesis Adapt to CO2-Enriched Environments? An Experiment on Plants Originating from Three Natural CO2 Springs. New Phytologist, 182, 698-709.
https://doi.org/10.1111/j.1469-8137.2009.02786.x

[73]   Ellsworth, D.S., Reich, P.B., Naumburg, E., Koch, G.W., Kubiske, M.E. and Smith, S.D. (2004) Photosynsis, Carboxylation and Leaf Nitroeng Responses of 16 Species to Elevated pCO2 across Four Free—Are CO2 Enrichment Experiments in Forest, Grassland and Desert. Global Change Biology, 10, 1-18.
https://doi.org/10.1111/j.1365-2486.2004.00867.x

[74]   Norby, R.J., Wullschleger, S.D., Gunderson, C.A., Johnson, D.W. and Ceulemans, R. (1999) Tree Responses to Rising CO2 in Field Experiments: Implications for the Future Forest. Plant Cell and Environment, 22, 683-714.
https://doi.org/10.1046/j.1365-3040.1999.00391.x

 
 
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