Abstract
Nitrogen cycling in northern temperate forest ecosystems could change under increasing atmospheric CO2 and tropospheric O3 as a result of quantitative and qualitative changes in plant litter production. At the Aspen Free Air CO2–O3 Enrichment (FACE) experiment, we previously found that greater substrate inputs to soil under elevated CO2 did not alter gross N transformation rates in the first 3 years of the experiment. We hypothesized that greater litter production under elevated CO2 would eventually cause greater gross N transformation rates and that CO2 effects would be nullified by elevated O3. Following our original study, we continued measurement of gross N transformation rates for an additional four years. From 1999 to 2003, gross N mineralization doubled, N immobilization increased 4-fold, but changes in microbial biomass N and soil total N were not detected. We observed year-to-year variation in N transformation rates, which peaked during a period of foliar insect damage. Elevated CO2 caused equivalent increases in gross rates of N mineralization (+34%) and NH +4 immobilization (+36%). These results indicate greater rates of N turnover under elevated CO2, but do not indicate a negative feedback between elevated CO2 and soil N availability. Elevated O3 decreased gross N mineralization (−16%) and had no effect on NH +4 immobilization, indicating reduced N availability under elevated O3. The effects of CO2 and O3 on N mineralization rates were mainly related to changes in litter production, whereas effects on N immobilization were likely influenced by changes in litter chemistry and production. Our findings also indicate that concomitant increases in atmospheric CO2 and O3 could lead to a negative feedback on N availability.
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References
Allen AS, Andrews JA, Finzi AC, Matamala R, Richter DD, Schlesinger WH. 2000. Effects of Free-air CO2 Enrichment (FACE) on belowground processes in a Pinus taeda Forest. Ecol Appl 10:437–48
Belovsky GE, Slade JB. 2000. Insect herbivory accelerates nutrient cycling and increases plant production. Proc Nat Acad Sci 97:14412–7
Bortier K, Ceulemans R, Temmerman L. 2000. Effects of tropospheric ozone on woody plants. Environmental Pollution and Plant Responses (Eds SB Agrawal & M Agrawal) 153–74
Cabrera ML, Beare MH. 1993. Alkaline persulfate oxidation for determining total nitrogen in microbial biomass extracts. Soil Sci Soc Am J 57:1007–1012
Ceulemans R, Mousseau M. 1994. Tansley Review No. 71. Effects of Elevated Atmospheric CO2 on Woody Plants. New Phyt 127:425–46
Chapman JA, King JS, Pregitzer KS, Zak DR. 2005. Effects of elevated atmospheric CO2 and tropospheric O3 on the decomposition of fine roots. Tree Phys In review
Cheng W. 1999. Rhizosphere feedbacks in elevated CO2. Tree Phys 19:313–20
Chung H, Zak DR, Lilleskov EA. 2005. Fungal community metabolism and composition are altered by plant growth under elevated CO2 and O3. Oecologia In review
Coleman MD, Dickson RE, Isebrands JG, Karnosky DF. 1995a. Photosynthetic productivity of aspen clones varying in sensitivity to tropospheric ozone. Tree Phys 15:585–92
Coleman MD, Dickson RE, Isebrands JG, Karnosky DF. 1995b. Carbon allocation and partitioning in aspen clones varying in sensitivity to tropospheric ozone. Tree Phys 15:593–604
Cotrufo M, Berg B, Kratz W. 1998. Increased atmospheric CO2 and litter quality. Env Review 6:1–12
Cotrufo MF, Ineson P. 1995. Effects of enhanced atmospheric CO2 and nutrient supply on the quality and subsequent decomposition fine roots of Betula pendula Roth. and Picea sitchensis (Bong.) Carr. Oecologia 106:525–30
Cotrufo MF, Ineson P. 1996. Elevated CO2 reduces field decomposition rates of Betula pendula (Roth.) leaf litter. Oecologia 106:525–30
Curtis PS, Wang X. 1998. A meta-analysis of elevated CO2 effects on woody plant mass, form, and physiology. Oecologia 113:299–313
Curtis PS, Vogel CS, Wang X, Pregitzer KS, Zak DR, Lussenhop J, Kubiske M, Teeri JA. 2000. Gas exchange, leaf nitrogen, and growth efficiency of Populus tremuloides in a CO2 enriched atmosphere. Ecol Appl 10:3–17
Davidson EA, Hart SC, Firestone MK. 1992. Internal cycling of nitrate in soils of a mature coniferous forest. Ecology 73:1148–56
Dickson RE, Lewin KF, Isebrands JG, others. 2000. Forest atmosphere carbon transfer storage-II (FACTS II) - The aspen free-air CO2 and O3 enrichment (FACE) project in an overview. USDA Forest Service North Central Experiment Station. General Technical Report NC-214 68 pp
Findlay S, Carreiro M, Krischik V, Jones CG. 1996. Effects of damage to living plants on leaf litter quality. Ecol Appl 6:269–75
Finlayson-Pitts BJ, Pitts JN Jr. 1997. Tropospheric air pollution: ozone, airborne toxics, polycyclic aromatic hydrocarbons, and particulates. Science 276:1045–51
Finzi AC, AS Allen EJ DeLucia DS Ellsworth WH Schlesinger. 2001. Forest litter production, chemistry and decomposition following two years of free-air CO2 enrichment. Ecology 82:470–84
Finzi AC, Schlesinger WH. 2003. Soil-Nitrogen Cycling in a Pine Forest Exposed to 5 Years of Elevated Carbon Dioxide. Ecosystems 6:444–56
Fog K. 1988. The effect of added nitrogen on the rate of decomposition of organic matter. Biological Reviews of the Cambridge Philosophical Society 63:433–62
Fowler D, Flechard C, Skiba U, Coyle M, Cape JN. 1998. The atmospheric budget of oxidized nitrogen and its role in ozone formation and deposition. New Phyt 139:11–23
Fowler D, Cape JN, Coyle M, Flechard C, Kuylenstierna J, Hicks K, Derwent D, Johnson C, Stevenson D. 1999. The global exposure of forests to air pollutants. Water Air Soil Pollution 116:5–32
Hart SC, Stark JM, Davidson EA, Firestone MK. 1994. ‘Nitrogen mineralization, immobilization, and nitrification’, in Methods of Soil Analysis Part 2 Microbiological and Biochemical Properties, Weaver RW, Angle S, Bottomley P, Bezdicek D, Smith S, Tabatabai A, Wollum A, ed. Soil Science Society of America, Segoe, Wisconsin, USA, pp 985–1018
Holmes WE, Zak DR, Pregitzer KS, King JS. 2003. Soil nitrogen transformations under Populus tremuloides, Betula papyrifera and Acer saccharum following 3 years exposure to elevated CO2 and O3. Global Change Biol 9:1743–50
Hoorens B, Aerts R, Stroetenga M. 2003. Is there a trade-off between the plant’s growth response to elevated CO2 and subsequent litter decomposability? OIKOS 103:17–30
Horwath WR, Paul EA. 1994. ‘Microbial Biomass’, in Methods of Soil Analysis Part 2 Microbiological and Biochemical Properties, Weaver RW, Angle S, Bottomley P, Bezdicek D, Smith S, Tabatabai A, Wollum A, ed.Soil Science Society of America, Segoe, Wisconsin, USA, pp 753–73
Hungate BA, Dijkstra P, Johnson DW, Hinkle CR, Drake BG. 1999. Elevated CO2 increases nitrogen fixation and decreases soil nitrogen mineralization in Florida scrub oak. Global Change Biol 5:781–9
Isebrands JG, McDonald EP, Kruger E, Hendrey GR, Pregitzer KS, Percy, Sober J, Karnosky DF. 2001. Growth responses of Populus tremuloides clones to interacting elevated carbon dioxide and tropospheric ozone. Env Pollution 115:359–71
Islam KR, Mulchi CL, Ali AA. 2000. Interactions of tropospheric CO2 and O3 enrichments and moisture variations on microbial biomass and respiration in soil. Global Change Biol 6:255–65
Johnson DW, Cheng W, Burke IC. 2000. Biotic and abiotic nitrogen retention in a variety of forest soils. Soil Sci Soc Am J 64:1503–14
Johnson DW, Cheng W, Joslin JD, Norby RJ, Edwards NT, Todd DE. 2004. Effects of elevated CO2 on nutrient cycling in a sweetgum plantation. Biogeochemistry 69:379–403
Kainulainen P, Holopainen T, Holopainen JK. 2003. Decomposition of secondary compounds from needle litter of Scots pine grown under elevated CO2 and O3. Global Change Biol 9:295–304
Karnosky DF, Gagnon ZE, Dickson RE, Coleman MD, Lee EH, Isebrands JG. 1996. Changes in growth, leaf abscission, and biomass associated with seasonal tropospheric ozone exposures of Populus tremuloides clones and seedlings. Can J For Res 16:23–27
Karnosky DF, Mankovska B, Percy K, et al. 1999. Effects of tropospheric O3 on trembling aspen and interaction with CO2: results from an O3-gradient and a FACE experiment. Water Air Soil Pollution 116:311–22
Karnosky DF, Zak DR, Pregitzer KS, et al. 2003. Low levels of tropospheric O3 moderate responses of temperate hardwood forests to elevated CO2: A synthesis of results from the Aspen FACE project. Functional Ecology 17:289–304
King JS, Pregitzer KS, Zak DR, Karnosky DF, Isebrands JG, Dickson RE, Hendrey GR, Sober J. 2001. Fine root biomass and fluxes of soil carbon in young stands of paper birch and trembling aspen is affected by elevated CO2 and tropospheric O3. Oecologia 128:237–50
King JS, Hanson PJ, Bernhardt E, DeAngelis P, Norby RJ, Pregitzer KS. 2004. A multiyear synthesis of soil respiration responses to elevated atmospheric CO2 from four forest FACE experiments. Global Change Biol 10:1027–42
King JS, Kubiske ME, Pregitzer KS, Hendrey GR, Quinn VS, Giardina C, McDonald EP, Karnosky DF. 2005a. Ozone decreases the capacity of CO2 fertilization of forests to offset fossil fuel emissions. Nature In review
King, JS, Pregitzer KS, Zak DR, Holmes WE, Schmidt K. 2005b. Fine root chemistry and decomposition in north-temperate tree species show little response to elevated atmospheric CO2 and varying soil N availability. Tree Phys In review
Larson J, Zak DR, Sinsabaugh RL. 2002. Extracellular enzyme activity and metabolism of root-derived substrates beneath temperate trees growing under elevated CO2 and O3. Soil Sci Soc Am J 66:1848–56
Lindroth RL, Kopper BJ, Parsons WFJ, et al. 2001. Consequences of elevated carbons dioxide and ozone for foliar chemical composition and dynamics in trembling aspen (Populus tremuloides) and paper birch (Betula papyrifera). Env Pollution 115:395–404
Liu L, King JS, Giardina CP. 2005. Effects of elevated atmospheric CO2 and tropospheric O3 on leaf litter production and chemistry in trembling aspen and paper birch ecosystems. Tree Phys In review
Loya WM, Pregitzer KS, Karberg NJ, King JS, Giardina CP. 2003. Reduction of soil carbon formation by tropospheric ozone under increased carbon dioxide levels. Nature 425:705–7
McDonald EP, Kruger EL, Riemenschneider DE, Isebrands JG. 2002. Competitive status influences tree-growth responses to elevated CO2 and O3 in aggrading aspen stands. Functional Ecology 16:792–801
Noormets A, McDonald EP, Kruger EL, Isebrands JG, Dickson RE, Karnosky DF. 2001. The effect of elevated carbon dioxide and ozone on leaf- and branch level photosynthesis and potential plant-level carbon gain in aspen. Trees 15:262–70
Norby RJ, Cotrufo MF, Ineson P, O’Neil EG, Canadell JG. 2001. Elevated CO2 litter chemistry and decomposition: a synthesis. Oecologia 127:153–65
Norby RJ, Hanson PJ, O’Neill EG, Tschaplinski TJ, Weltzin JF, Hansen RT, Cheng W, Wullschleger SD, Gunderson CA, Edwards NT, Johnson DW. 2002. Net primary productivity of a CO2-enriched deciduous forest and the implications for carbon storage. Ecol Appl 12:1261–6
Oren R, Ellsworth DS, Johnson KH, et al. 2001. Soil fertility limits carbon sequestration by a forest ecosystem in a CO2-enriched atmosphere. Nature 411:469–72
Paul EA, Morris SJ, Six J, Paustian K, Gregorich EG. 2003. Interpretation of soil carbon and nitrogen dynamics in agricultural and afforested soils. Soil Sci Soc Am J 67:1620–8
Percy KE, Awmack CS, Lindroth RL, Kubiske ME, Kopper BJ, Isebrands JG, Pregitzer KS, Hendrey GR, Dickson RE, Zak DR, and others. 2002. Nature 420:403–7
Phillips RL, Zak DR, Holmes WE, White DC. 2002. Microbial community composition and function beneath temperate trees exposed to elevated atmospheric carbon dioxide and ozone. Oecologia 131:236–44
Pregitzer KS, Loya WM, Kubiske ME, and Zak DR. 2006. Soil respiration in northern forests exposed to elevated atmospheric carbon dioxide and ozone. Oecologia In press
Scherzer AJ, Rebbeck J, Boerner REJ. 1998. Foliar nitrogen dynamics and decomposition of yellow-poplar and eastern white pine during four seasons of exposure to elevated ozone and carbon dioxide. For Ecol Management 109:355–66
Wan S, Norby RJ, Pregitzer KS, Ledford J, O’Neil EG. 2004. CO2 enrichment and warming of the atmosphere enhance both productivity and mortality of maple tree fine roots. New Phyt 162:437–46
Zak DR, Pregitzer KS, Curtis PS, Teeri JA, Fogel R, Randlett DL. 1993. Elevated atmospheric CO2 and feedback between carbon and nitrogen cycles. Plant Soil 151:105–17
Zak DR, Pregitzer KS, King JS, Holmes WE. 2000a. Elevated atmospheric CO2, fine roots and the response of soil microorganisms: a review and hypothesis. New Phyt 147:201–22
Zak DR, Pregitzer KS, Curtis PS, Vogel CS, Holmes WE, Lussenhop J. 2000b. Atmospheric CO2, soil-N availability, and allocation of biomass and nitrogen by Populus tremuloides. Ecol Appl 10:34–46
Zak DR, Holmes WE, Finzi AC, Norby RJ, Schlesinger WH. 2003. Soil nitrogen cycling under elevated CO2: A synthesis of forest face experiments. Ecol Appl 13:1508–14
Acknowledgements
We thank Matt Tomlinson, Jana Gastellum, Michelle Martin, Andrea Firman, Beth Christensen, and Nicole Tuttle for assisting in the field and laboratory. Dave Karnosky, Judd Isebrands, Jaak Sober and Wendy Jones provided logistical support by maintaining the Aspen FACE experiment. Aspen FACE is principally supported by the Office of Science (BER), U.S. Department of Energy (DE-FG02-95ER62125), the U.S. Forest Service Northern Global Change Program and North Central Research Station, Michigan Technological University, and Natural Resources Canada – Canadian Forest Service.
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Holmes, W.E., Zak, D.R., Pregitzer, K.S. et al. Elevated CO2 and O3 Alter Soil Nitrogen Transformations beneath Trembling Aspen, Paper Birch, and Sugar Maple. Ecosystems 9, 1354–1363 (2006). https://doi.org/10.1007/s10021-006-0163-5
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DOI: https://doi.org/10.1007/s10021-006-0163-5
Keywords
- Acer saccharum
- Betula papyrifera
- Carbon dioxide
- FACE
- Gross N immobilization
- Gross N mineralization
- Microbial biomass
- Nitrogen cycling
- Ozone
- Populus tremuloides