Progress 10/01/00 to 09/30/05
Outputs OUTPUTS: Forest Response to Elevated Carbon Dioxide and Ozone - Anthropogenic ozone and carbon dioxide induced declines in soil N availability could counteract greater plant growth in a carbon dioxide-enriched atmosphere, thereby reducing net primary productivity (NPP) and the potential of terrestrial ecosystems to sequester anthropogenic carbon dioxide. Presently, it is uncertain how increasing atmospheric carbon dioxide and ozone will alter plant N demand, the acquisition of soil N by plants as well as the microbial supply of N from soil organic matter. To address this uncertainty, we initiated an ecosystem-level 15N tracer experiment at the Rhinelander Free Air carbon dixoide - ozone Enrichment (FACE) facility to understand how projected increases in atmospheric carbon dixoide and ozone alter the distribution and flow of N in developing northern temperate forests. Tracer amounts of 15N were applied to the forest floor of FACE rings in which developing Populus tremuloides and P. tremuloides-Betula papyrifera communities have been exposed to factorial carbon dixoide and ozone treatments for 7 years. We also have conducted many biogeochemical analyses to better understand how soil carbon and nitrogen cycling will be altered by these trace gases. Forest Response to Atmospheric Nitrogen Deposition - Forest floor and soil organic matter are the least certain aspects of C storage in northern forests, and there are reasons to expect that atmospheric N deposition could influence these pools by means other than greater rates of NPP and detritus production. For unknown reasons, the synthesis of lignolytic enzymes by some litter-decomposing fungi can be repressed by high levels of inorganic N, which can, in turn, slow decomposition and increase soil organic matter accumulation. Other empirical evidence demonstrates that the later stages of litter decomposition, which are dominated by lignin degradation, are slowed in detritus with a high initial N concentration. If atmospheric N deposition increases leaf litter N and elevates inorganic N in soil solution, then it could repress lignolytic activity, slow organic matter decomposition, and increase soil C storage. To the best of our knowledge, these specific mechanisms are not considered by the majority biogeochemical model simulating the influence of atmospheric N deposition on ecosystem C storage, and they could have a substantial influence on organic matter accumulation in the forest floor and mineral soil of forests in the Northern Hemisphere. Our objective was to determine if experimental N deposition has altered organic matter and N stored in northern hardwood forests, especially in forest floor and mineral soil. Dissemination to Communities of Interest - We have disseminated the new knowledge we have generated to the community of scientists who are working to better understand how forest ecosystems will respond to climate change. We have accomplished this by actively publishing our work in the scientific literature, by presenting our research at national and international scientific meetings, and by training a new generation of scientists to address these pressing ecological issues. PARTICIPANTS: Nothing significant to report during this reporting period. TARGET AUDIENCES: Nothing significant to report during this reporting period. PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.
Impacts Forest Response to Elevated Carbon Dioxide and Ozone - Tracer amounts of 15N were applied to the forest floor of developing Populus tremuloides and P. tremuloides-Betula papyrifera communities have been exposed to factorial carbon dioxide and O3 treatments for 7 years. One year after isotope addition, both forest communities exposed to elevated carbon dioxide obtained greater amounts of N (40%) and 15N (29%) from soil, despite no change in soil N availability or plant N-use efficiency. Elevated carbon dioxide increased the ability of plants to exploit soil for N, through the development of a larger root system. Conversely, elevated ozone decreased the amount of N (-29%) and 15N (-15%) in both communities. The diminished demand for soil N resulted from of leaf damage, declines in photosynthesis, and lower growth. Neither carbon dioxide nor ozone altered the amount of N or the distribution of 15N in any soil pools. In a carbon dioxide -enriched atmosphere, greater belowground growth and a more thorough exploitation of soil for growth limiting N is an important mechanism sustaining the enhancement of NPP in developing forests. However, as carbon dioxide accumulates in the Earth's atmosphere, future ozone concentrations threaten to diminish the enhancement of plant growth, decrease plant N acquisition, and lessen the storage of anthropogenic C in temperate forests. Forest Response to Atmospheric Nitrogen Deposition - We constructed organic matter and N budgets for replicate northern hardwood stands (n = 4) which have received ambient and experimental N deposition (ambient plus 3 g nitrate-N m-2 y-1) for a decade; we also traced the flow of a 15N- pulse over a 6-year period. Experimental N deposition had no effect on organic matter or N stored in the standing forest overstory, but it did significantly increase the N concentration (+19%) and N content (+24%) of canopy leaves. In contrast, a decade of experimental NO3- deposition significantly increased amounts of organic matter (+12%) and N (+9%) in forest floor and mineral soil, despite no increase in detritus production. A greater forest floor (Oe/a) mass under experimental NO3- deposition resulted from slower decomposition, which is consistent with previously reported declines in lignolytic activity by microbial communities exposed to experimental N deposition. Tracing 15N revealed that N accumulated in soil organic matter by first flowing through soil microorganisms and plants, and that the shedding of 15N-labeled leaf litter enriched soil organic matter over a 6-year duration. Our results demonstrate that atmospheric N deposition exerts a direct and negative effect on microbial activity in this forest ecosystem, slowing the decomposition of aboveground litter and leading to the accumulation of forest floor and soil organic matter. To the best of our knowledge, this mechanism is not represented in the majority of simulation models predicting the influence of anthropogenic N deposition on ecosystem C storage in northern forests
Publications
- Rothstein, D.E., D.R. Zak, K.S. Pregitzer, P.S. Curtis. 2000. Kinetics of nitrogen uptake by Populus tremuloides in relation to atmospheric CO2 and soil nitrogen availability. Tree Physiology 20: 265-270.
- Zak, D.R., K.S. Pregitzer, J.S. King, and W.E. Holmes. 2000. Elevated atmospheric CO2, fine roots and the response of soil microorganisms: a review and hypothesis. New Phytologist 147: 201-222.
- Mikan, C.J., D.R. Zak, M.E. Kubiske, and K.S. Pregitzer. 2000. Combined effects of atmospheric CO2 and N availability on the belowground carbon and nitrogen dynamics of aspen mesocosms. Oecologia 124:432-445.
- Wang, X.Z., P.S. Curtis, K.S. Pregitzer, and D.R. Zak. 2000. Genotypic variation in physiological and growth responses of Populus tremuloides to elevated atmospheric CO2 concentration. Tree Physiology 20: 1019-1028.
- King, J.S., K.S. Pregitzer, D.R. Zak, M.E. Kubiske, J.A. Ashby, and W.E. Holmes. 2001. Chemistry and decomposition of litter from Populus tremuloides Michaux grown at elevated atmospheric CO2 and varying N availability. Global Change Biology 7: 65-74.
- King J.S., K.S. Pregitzer, D.R. Zak D.F. Karnosky, I.G. Isebrands, R.E. Dickson, G.R. Hendrey, J. Sober. 2001. Fine root biomass and fluxes of soil carbon in young stands of paper birch and trembling aspen as affected by elevated atmospheric CO2 and tropospheric O3. Oecologia 128:237-250.
- King, J.S., K.S. Pregitzer, D.R. Zak, M.E. Kubiske, W.E. Holmes. 2001. Correlation of foliage and litter chemistry of sugar maple, Acer saccharum, as affected by elevated CO2 and varying N availability, and effects on decomposition. Oikos 94: 403-416
- Fisk, M., D.R. Zak, and T.R. Crow. 2002. Nitrogen storage and cycling in old- and second-growth northern hardwood forests. Ecology 83:73-87.
- Phillips, R.L., D.R. Zak, and W.E. Holmes, and D.C. White. 2002. Microbial community composition and function beneath temperate trees exposed to elevated atmospheric CO2 and O3. Oecologia 131:236-244.
- Kubiske, M.E., D.R. Zak, K.S. Pregitzer, Y. Takeuchi. 2002. Three years of photosynthetic acclimation to elevated atmospheric CO2: overstory Populus tremuloides and understory Acer saccharum: interactions with shade and soil N. Tree Physiology 22: 321-329.
- Percy, K.E., C. S. Awmack, R. L. Lindroth, M.E. Kubiske, B.J. Kopper, J.G. Isebrands, K.S. Pregitzer, G.R. Hendrey, R.E. Dickson, D.R. Zak, E. Oksanen, J. Sober, R. Harrington, & D.F. Karnosky. 2002. Altered performance of forest pests under CO2- and O3 - enriched atmospheres. Nature 420: 403-407.
- Saiya-Cork, K.R., R. L. Sinsabaugh, and D. R. Zak. 2002. The effects of long-term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biology & Biochemistry 34: 1309-1315.
- Davidson, E.A., K. Savage, P. Bolstad, D.A. Clark, P.S. Curtis, D.S. Ellsworth, P.J. Hanson, B.E. Law, Y. Luo, K.S. Pregitzer, J.C. Randolph, D.R. Zak. 2002. Belowground carbon allocation in forests estimated from litterfall and IRGA-based soil respiration measurements. Forest and Agricultural Meterology 113: 39-51.
- Larson, J.L., D.R. Zak, and R.L. Sinsabaugh. 2002. Microbial activity beneath temperate trees growing under elevated CO2 and O3. Soil Science Society of America 66:1848-1856.
- Karnosky, D.F., D.R. Zak, K.S. Pregitzer, C.S. Awmack, J.G. Bockheim, R.E. Dickson, G.R. Hendrey, G.E. Host, J.S. King, B.J. Kopper, E.L. Kruger, M.E. Kubiske, R.L. Lindroth, W.J. Mattson, E.P. McDonald A. Noormets, E. Oksanen, W.F.J. Parsons, K.E. Percy, G.K. Podila, D.E. Riemenschneider, P. Sharma, A. Sober, J. Sober, W.S. Jones, S. Anttonen, E. Vapaavuori, and J.G. Isebrands. 2003. Tropospheric O3 moderates responses of temperate hardwood forests to elevated CO2: A synthesis of molecular to ecosystem results from the Aspen FACE project. Functional Ecology 17:287-307.
- Williams, E.L., L.M. Walter, T.C.W. Ku, G.W. Kling, and D.R. Zak. 2003. CO2 and nutrient availability effects on mineral weathering. Global Biogeochemcal Cycles 17 (2): Art. No. 1041.
- Holmes, W.E., D.R. Zak, K.S. Pregitzer, and J.S. King. 2003. Nitrogen cycling beneath Populus tremuloides, Betula papyrifera and Acer saccharum growing under elevated CO2 and O3. Global Change Biology 9: 1743-1750.
- Sinsabaugh, R.L., K. Saiya-Cork, T. Long, M.P. Osgood, D. Neher, D.R. Zak, and R.J. Norby. 2003. Soil microbial activity in a Liquidambar plantation unresponsive to CO2-driven increases in primary production. Applied Soil Ecology 24:263-271.
- Zak, D.R., W.E. Holmes, A.C. Finzi, R.J. Norby, and W.H. Schlesinger. 2003. Soil nitrogen cycling under elevated CO2: a synthesis of forest FACE experiments. Ecological Applications 13: 1051-1061.
- DeForest, J.L., D.R. Zak, K.S. Pregitzer, and A.J. Burton. 2004. Experimental NO3- additions alter microbial community function in northern hardwood forests. Soil Science Society of America Journal 68: 132-138.
- Gallo, M., R. Amonette, C. Lauber, R.L. Sinsabaugh and D.R. Zak. 2004 Microbial community structure and oxidative enzyme activity in nitrogen-amended north temperate forest soils. Microbial Ecology 48: 218-229
- DeForest, J.L., D.R. Zak, K.S. Pregitzer and A.J. Burton. 2005. Atmospheric NO3- deposition, declines in decomposition and increases in DOC: Test of a potential mechanism. Soil Science Society of America Journal 69: 1233-1237.
- Karnosky, D.R., K.S. Pregitzer, D.R. Zak M.E. Kubiske, G.R. Hendrey, D. Weinstein, and K.E. Percy. 2005. Scaling ozone responses of forest trees to the ecosystem level. Plant, Cell & Environment. 28: 965-981. Gallo, M.E., C.L. Lauber, S.E Cabaniss, M. Waldrop, R.L. Sinsabaugh and
- D.R. Zak. 2005. Soil organic matter and litter chemistry response to experimental N deposition in northern temperate deciduous forest ecosystems. Global Change Biology 11: 1514-1521.
- Chapman, J.A., J.S. King, K.S. Pregitzer, and D.R. Zak, 2005. Effects of elevated CO2 and tropospheric O3 on the decomposition of fine roots. Tree Physiology 25: 1501-1510.
- Sinsabaugh, R.L., M.E. Gallo , C. Lauber , M.P Waldrop, and D.R. Zak.2005. Extracellular enzyme activities and soil carbon dynamics for northern hardwood forests receiving simulated nitrogen deposition. Biogeochemistry 75: 201-215.
- DeForest, J.L., D.R. Zak, K.S. Pregitzer, and A.J. Burton. 2004. Nitrate deposition and the microbial degradation of cellulose and lignin in a northern hardwood forest. Soil Biology & Biochemistry 36: 965-971.
- Pregitzer, K.S., D.R. Zak, A.J. Burton, and J.A. Ashby. 2004. Chronic nitrate additions dramatically increase the export of carbon and nitrogen in northern hardwood forests. Biogeochemistry 68: 179-197.
- Zak, D.R., K.S. Pregitzer, W.E. Holmes, A.J. Burton and G.P. Zogg. 2004. Anthropogenic N deposition and the fate of 15NO3- in a northern hardwood ecosystem. Biogeochemistry 69: 143-157.
- Burton, A.J., K.S. Pregitzer, J.N. Crawford, G.P. Zogg, and D.R. Zak. 2004. Chronic NO3- additions reduce soil respiration in northern hardwood forests. Global Change Biology 10: 1080-1091.
- Waldrop, M.P., D.R. Zak, and R.L. Sinsabaugh. 2004. Microbial community response to nitrogen deposition in northern forest ecosystems. Soil Biology & Biochemistry 36: 1443-1451.
- Sinsabaugh, R.L., D.R. Zak, M. Gallo, C. Lauber, and A. Amonette. 2004. Nitrogen deposition and dissolved organic carbon production in northern temperate forests. Soil Biology & Biochemistry 36:1509-1515.
- Waldrop, M.P., D.R. Zak, R.L. Sinsabaugh, M. Gallo, and C. Lauber. 2004. Nitrogen deposition modifies soil carbon storage through changes in microbial enzyme activity. Ecological Applications 14: 1172-1177.
- Luo Y, B. Su, W. S. Currie, J. S. Dukes, A. Finzi, U. Hartwig, B. Hungate, R. McMurtrie, R. Oren, W. J. Parton, D. Pataki, R. Shaw, D. R. Zak, and C. Field. 2004. Progressive nitrogen limitation of ecosystem responses to rising atmospheric CO2. BioScience 54:731-739.
- Pregitzer, K.S., W.M. Loya, M.E. Kubiske, and D.R. Zak. 2006. Soil respiration in northern forests exposed to elevated atmospheric carbon dioxide and ozone. Oecologia 148: 503-516.
- Chung, H., D.R. Zak, and E.A Lilleskov. 2006. Fungal community metabolism and composition are altered by plant growth under elevated CO2 and O3. Oecologia 147: 143-154.
- Zak, D.R., W.E. Holmes, M.J. Tomlinson, K.S. Pregitzer, and A.J. Burton. 2006. Microbial cycling of C and N in northern hardwood forests receiving chronic atmospheric NO3- deposition. Ecosystems 9:242-253.
- Zak, D.R., C.B. Blackwood, and M.P. Waldrop. 2006. A molecular dawn for biogeochemistry. Trends in Ecology & Evolution 21: 288-295.
- Bandeff, J.M., K.S. Pregitzer, W.M. Loya, W.E. Holmes, and D.R. Zak. 2006. The effects of elevated atmospheric CO2 and O3 on understory species composition and nitrogen acquisition. Plant and Soil 282: 251-259.
- Smemo, K.A., D.R. Zak, and K.S. Pregitzer. 2006. Chronic NO3- deposition reduces the retention of fresh leaf litter-derived DOC in northern hardwood forests. Soil Biology & Biochemistry 38: 1340-1347.
- Sefcik, L.T., D.R. Zak and D.S. Ellsworth. 2006. Photosynthetic responses to understory shade and elevated CO2 in four northern hardwood tree species. Tree Physiology 25: 1589-1599.
- Waldrop, M.P, and D.R. Zak. 2006. Microbial mechanisms controlling dissolved organic carbon production in response to elevated atmospheric nitrogen deposition. Ecosystems 9: 921-933
- Antibus, R.K., C. Lauber, R.L. Sinsabaugh, and D.R. Zak. 2006. Responses of Bradford reactive soil protein to experimental nitrogen addition in three forest communities in northern Lower Michigan. Plant and Soil 288: 173-187.
- Holmes, W.E., D.R. Zak, K.S. Pregitzer, and J.S. King. 2006. Elevated CO2 and O3 alter soil nitrogen transformations beneath trembling aspen, paper birch, and sugar maple. Ecosystems 9: 1354-1363.
- Chung, H., D.R. Zak, D.S. Ellwsorth, and P.B. Reich. 2007. Plant diversity, elevated CO2 and atmospheric N deposition alter microbial community composition and function. Global Change Biology 13: 980-989.
- King, J.S., K.S. Pregitzer, D.R. Zak, W.E. Holmes, and K. Schmidt. 2006. Fine root chemistry and decomposition in north-temperate tree species show little response to elevated atmospheric CO2 and varying soil N availability. Oecologia 146: 318-328.
- Sefcik, L.T., D.R. Zak and D.S. Ellsworth. 2007. Seedling survival is increased by elevated atmospheric CO2. Global Change Biology 13: 132-146.
- Blackwood, C.B., M.P. Waldrop, D.R. Zak and R.L. Sinsabaugh. 2007. Molecular analysis of fungal communities and laccase genes in decomposing litter reveal differences among forest types but no impact of N deposition. Environmental Microbiology 9: 1306-1316.
- Blackwood, C.B., D.E. Hudleston, D.R. Zak and J.S. Buyer. 2007. Interpreting ecological diversity indices applied to T-RFLP data: insights from simulated microbial communities. Applied and Environmental Microbiology 73: 5276-5283.
- Zak, D.R., W.E. Holmes, K.S. Pregitzer, J.S. King, D.S. Ellsworth, and M.E. Kubiske. 2007. Belowground composition and the response of developing forest communities to atmospheric CO2 and O3. Global Change Biology 13: 2230-2238.
- Finzi, A.C., R.J. Norby, C. Calfapietrac, A. Gallet-Budyneka, B. Gielend, W.E. Holmes, M.R. Hoosbeek, C.M. Iversen, R.B. Jackson, M.E. Kubiske, J. Ledford, M. Liberloo, R. Oren, A. Polle, S. Pritchard, D.R. Zak, and R. Ceulemans. 2007. Increases in nitrogen uptake rather than nitrogen-use efficiency support high rates of temperate forest productivity under elevated CO2. Proceeding of the National Academy of Sciences 104: 14014-14019.
- Smemo, K.A., D.R. Zak, K.S. Pregitzer, and A.J. Burton. 2007. Characteristics of DOC exports from northern hardwood forests receiving chronic atmospheric NO3- deposition. Ecosystems 10: 369-379.
- Zak, D.R., W.E. Holmes, and K.S. Pregitzer. 2007. Atmospheric CO2 and O3 alter the flow of 15N in developing forest ecosystems. Ecology 88: 2630-2639.
- Hofmockel, K.S., D.R. Zak and C.B. Blackwood. 2007. Does atmospheric N deposition alter the abundance and activity of lignolytic fungi in forest soils Ecosystems 10: 1278-1286.
- Pregitzer, K.S., A.J. Burton, D.R. Zak, and A.F. Talhelm. 2008. Simulated chronic N deposition increases carbon storage in northern temperate forests. Global Change Biology 14: 142-153.
- Lesaulnier, C., D. Papamichail, S. McCorkle, B. Ollivier, S. Skiena, S. Taghavi, D.R. Zak, and D. van der Lelie. 2008. Elevated CO2 affects soil microbial diversity associated with trembling aspen. Environmental Microbiology 10: 926-941.
- Talhelm, A.F., K.S. Pregitzer, and D.R. Zak. 2009. Species-specific responses to atmospheric CO2 and O3 mediate changes in soil carbon. Ecology Letters. 12: 1-10.1091.
- DeForest, J.L., D.R. Zak, K.S. Pregitzer, and A.J. Burton. 2004. Nitrate deposition and the microbial degradation of cellulose and lignin in a northern hardwood forest. Soil Biology & Biochemistry 36: 965-971.
- Pregitzer, K.S., A.J. Burton, J.S. King and D.R. Zak. 2008. Soil respiration, root biomass, and root turnover following long-term exposure of northern forests to elevated atmospheric carbon dioxide and tropospheric ozone. New Phytologist 180: 153-161.
- Eddy, W.E., D.R. Zak, W.E. Holmes, and K.S. Pregitzer. 2008. Chronic NO3- deposition does not induce NO3- use by Acer saccharum Marsh. Ecosystems 11: 469-477.
- Hassett, J.E., D.R. Zak, C.B. Blackwood, and K.S. Pregitzer. 2009. Are basidiomycete laccase gene abundance and composition related to reduced lignolytic activity under elevated atmospheric NO3− deposition in a northern hardwood forest Microbial Ecology 57: 728-739.
- Kellner, H., and D.R. Zak. 2009. Expression of fungal type I polyketide synthase genes in a forest soil. Soil Biology and Biochemistry 41: 1344-1347.
- Chung, H., D.R. Zak, and P.B. Reich. 2009. Microbial assimilation of new photosynthate is altered by plant species richness and nitrogen deposition. Biogeochemistry 94: 233-242.
- Grandy, A.S., R.L. Sinsabaugh, J.C. Neff, M. Stursova, and D.R. Zak. 2008. Nitrogen deposition effects on soil organic matter chemistry are linked to variation in enzymes, ecosystems and size fractions. Biogeochemistry 91: 37-49.
- Waldrop, M.P., D.R. Zak, and R.L. Sinsabaugh. 2004. Microbial community response to nitrogen deposition in northern forest ecosystems. Soil Biology & Biochemistry 36: 1443-1451
- Sinsabaugh, R.L., C.L. Lauber, M.N. Weintraub, B. Ahmed, S.D. Allison, C. Crenshaw, AR. Contosta, D. Cusack, S. Frey, M. E. Gallo, T. B. Gartner, S.E. Hobbie, K. Holland, B.L. Keeler, J.S. Powers, M. Stursova, C. Takacs-Vesbach, M.P. Waldrop, M. Wallenstein D.R. Zak, L.H. Zeglin. 2008. Stoichiometry of soil enzyme activity at global scale. Ecology Letters 11: 1252-1264.
- Lauber, C.L., R.L. Sinsabaugh, and D.R. Zak. 2008. Laccase gene composition and relative abundance in oak forest soil is not affected by short-term nitrogen fertilization. Microbial Ecology 57: 50-57.
- Zak, D.R., W.E. Holmes, A.J. Burton, K.S. Pregitzer and A.F. Talhelm. 2008. Atmospheric NO3- deposition increases soil organic matter by slowing decomposition in a northern hardwood ecosystem. Ecological Applications 18: 2016-2027.
- Cutis, P.S., C.S. Vogel, X. Wang, K.S. Pregtizer, D.R. Zak, M.E. Kubiske, and J.A. Teeri. 2000. Gas exchange, leaf nitrogen, and growth efficiency of Populus tremuloides in a CO2 enriched atmosphere. Ecological Applications10: 3-17.
- Pregitzer. K.S., D.R. Zak, J. Maziasz, J. DeForest, P.S. Curtis, and J. Lussenhop. 2000. Interactive effects of atmospheric CO2 and soil-N availability on fine roots of Populus tremuloides. Ecological Applications 10: 18-33.
- Zak, D.R., K.S. Pregitzer, P.S. Curtis, C.S. Vogel, W.E. Holmes, and J. Lussenhop. 2000. Atmospheric CO2, soil N availability, and the allocation of biomass and nitrogen in Populus tremuloides. Ecological Applications 10: 34-46.
- Zak, D.R., K.S. Pregitzer, P.S. Curtis, and W.E. Holmes. 2000. Atmospheric CO2 and the composition and function of soil microbial communities. Ecological Applications 10: 47-59.
- Zogg, G.P., D.R. Zak, K.S. Pregitzer, and A.J. Burton. 2000. Microbial immobilization and the retention of anthropogenic nitrate in northern hardwood forests. Ecology 81: 1858-1866.
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