Belowground factors mediating changes in methane consumption in a forest soil under elevated CO2

[1] The sustained increase in atmospheric CO2 concentration observed over the past century, and projected to continue into the next, is of great significance for atmospheric CH4. Effects of elevated CO2 on microbial methane cycling are potentially mediated by its effects on plant physiology, which include enhancement of carbon assimilation, belowground carbon allocation, and water use efficiency. To determine the importance of such changes for methane cycling, belowground factors impacting soil CH4 consumption were investigated at the Free Air Carbon Transfer and Storage (FACTS)-I site in the Duke Forest, North Carolina, in which plots have been exposed to ambient (370 ppm) or elevated (ambient + 200 ppm) CO2 since August 1996. CH4 fluxes at the soil surface, porespace concentrations of CH4, O2, and CO2, soil moisture, soil temperature, and soil pH were simultaneously measured over 24 months. Porespace CH4 concentrations were highest (1.98 ± 0.25 ppm) at the soil surface and decreased to 0.65 ± 0.22 ppm at 30 cm, indicating that methanotrophic activity was depleting CH4 in the upper soil layers and creating a gradient to draw atmospheric CH4 into the soil. This was confirmed by surface CH4 flux measurements, which averaged −1.54 ± 0.65 μmol/m2/h. Under elevated CO2, porespace CH4 was 25–30% higher in the upper 70 cm of soils; CH4 fluxes from the atmosphere into soil were diminished by ∼25%; soil CO2 increased by 10–70%; and volumetric soil moisture was greater by up to 40% during some seasons. Statistical modeling revealed that soil moisture strongly predicted variability in surface CH4 fluxes and that soil CO2 and soil moisture both predicted variability in soil CH4. Results also indicated that a portion of the net CH4 sink inhibition in elevated CO2 soils could be attributable to alterations in soil biological processes, suggesting that changes in the CH4-cycling microbial ecology had taken place.

[1]  Berman D. Hudson,et al.  Soil organic matter and available water capacity , 1994 .

[2]  W. V. Lierop.  Soil pH and lime requirement determination. , 1990 .

[3]  C. Körner,et al.  Responses of soil microbiota of a late successional alpine grassland to long term CO2 enrichment , 1996, Plant and Soil.

[4]  J. A. Simmons,et al.  Methane and carbon dioxide dynamics in a northern hardwood ecosystem , 1995 .

[5]  R. Conrad,et al.  Oxidation of atmospheric methane in soil: Measurements in the field, in soil cores and in soil samples , 1993 .

[6]  G. Katul,et al.  WATER BALANCE DELINEATES THE SOIL LAYER IN WHICH MOISTURE AFFECTS CANOPY CONDUCTANCE , 1998 .

[7]  R. Knowles,et al.  Growth of methanotrophs in methane and oxygen counter gradients , 1995 .

[8]  M. Herlihy.  Distribution of nitrifying and heterotrophic microorganisms in cutover peats , 1973 .

[9]  M. R. Carter,et al.  Chapter 2 Physical attributes of soil quality , 1997 .

[10]  J. Guehl,et al.  Leaf gas exchange and carbon isotope composition responses to drought in a drought‐avoiding (Pinus pinaster) and a drought‐tolerant (Quercus petraea) species under present and elevated atmospheric CO2 concentrations , 1996 .

[11]  F. Day,et al.  Effects of elevated atmospheric CO2 on root decomposition in a scrub oak ecosystem , 2001 .

[12]  D. Ellsworth,et al.  Leaf and canopy responses to elevated CO2 in a pine forest under free-air CO2 enrichment , 1995, Oecologia.

[13]  P. Dunfield,et al.  Methane production and consumption in temperate and subarctic peat soils: Response to temperature and pH , 1993 .

[14]  Christopher B. Field,et al.  Stomatal responses to increased CO2: implications from the plant to the global scale , 1995 .

[15]  P. Curtis,et al.  Atmospheric CO2, soil nitrogen and turnover of fine roots , 1995 .

[16]  L. Lekkerkerk,et al.  Carbon Fluxes in Plant-Soil Systems at Elevated Atmospheric CO2 Levels. , 1991, Ecological applications : a publication of the Ecological Society of America.

[17]  D. Ellsworth.  CO2 enrichment in a maturing pine forest: are CO2 exchange and water status in the canopy affected? , 1999 .

[18]  R. Teskey.  A field study of the effects of elevated CO2 on carbon assimilation, stomatal conductance and leaf and branch growth of Pinus taeda trees , 1995 .

[19]  G. King,et al.  Response of Atmospheric Methane Consumption by Maine Forest Soils to Exogenous Aluminum Salts , 2000, Applied and Environmental Microbiology.

[20]  R. Mancinelli.  The regulation of methane oxidation in soil. , 1995, Annual review of microbiology.

[21]  B. Sitaula,et al.  CH4 uptake by temperate forest soil: Effect of N input and soil acidification , 1995 .

[22]  J. Lelieveld,et al.  Climate effects of atmospheric methane , 1993 .

[23]  John D. Alexander,et al.  Plant water relations and the effects of elevated CO2: a review and suggestions for future research , 1993 .

[24]  A. Knapp,et al.  Water vapour fluxes and their impact under elevated CO2 in a C4‐tallgrass prairie , 1997 .

[25]  G. King.  Responses of atmospheric methane consumption by soils to global climate change , 1997 .

[26]  T. L. Lyon,et al.  The Nature and Properties of Soils , 1930 .

[27]  William H. Schlesinger,et al.  Limited carbon storage in soil and litter of experimental forest plots under increased atmospheric CO2 , 2001, Nature.

[28]  J. Vose,et al.  Soil pCO?, soil respiration, and root activity in CCVfumigated and nitrogen-fertilized ponderosa pine , 2004 .

[29]  B. Drake,et al.  MORE EFFICIENT PLANTS: A Consequence of Rising Atmospheric CO2? , 1997, Annual review of plant physiology and plant molecular biology.

[30]  P. Crill.  Seasonal patterns of methane uptake and carbon dioxide release by a temperate woodland soil , 1991 .

[31]  G. King,et al.  Effects of Temperature on Methane Consumption in a Forest Soil and in Pure Cultures of the Methanotroph Methylomonas rubra , 1992, Applied and environmental microbiology.

[32]  Finzi,et al.  Net primary production of a forest ecosystem with experimental CO2 enrichment , 1999, Science.

[33]  I. Levin,et al.  Methane consumption in aerated soils of the temperate zone , 1990 .

[34]  G. Berntson,et al.  Regenerating temperate forest mesocosms in elevated CO2: belowground growth and nitrogen cycling , 1997, Oecologia.

[35]  W. Schlesinger,et al.  Enhanced CH4 emission from a wetland soil exposed to Elevated CO2 , 1997 .

[36]  W. Verstraete,et al.  Agricultural factors affecting methane oxidation in arable soil , 1996, Biology and Fertility of Soils.

[37]  E. Davidson,et al.  Land-Use Change and Biogeochemical Controls of Methane Fluxes in Soils of Eastern Amazonia , 2000, Ecosystems.

[38]  J. Morison,et al.  Sensitivity of stomata and water use efficiency to high CO2 , 1985 .

[39]  J. Almeida,et al.  Consequences of Rising Atmospheric Carbon Dioxide Levels for the Belowground Microbiota Associated with White Oak , 1997 .

[40]  R. Conrad.  Compensation concentration as critical variable for regulating the flux of trace gases between soil and atmosphere , 1994 .

[41]  R. Phillips,et al.  Response of soil methanotrophic activity to carbon dioxide enrichment in a North Carolina coniferous forest , 2001 .

[42]  A. Stein,et al.  Spatial variability of methane, nitrous oxide, and carbon dioxide emissions from drained grasslands. , 1998 .

[43]  G. L. Hutchinson,et al.  Improved Soil Cover Method for Field Measurement of Nitrous Oxide Fluxes , 1981 .

[44]  R. Striegl,et al.  Methane flux in subalpine wetland and unsaturated soils in the southern Rocky Mountains , 1999 .

[45]  Harry Vereecken,et al.  ESTIMATING THE SOIL MOISTURE RETENTION CHARACTERISTIC FROM TEXTURE, BULK DENSITY, AND CARBON CONTENT , 1989 .

[46]  Peter S. Curtis,et al.  A meta‐analysis of leaf gas exchange and nitrogen in trees grown under elevated carbon dioxide , 1996 .

[47]  P. Ambus,et al.  Nitrogen turnover rates in a riparian fen determined by 15N dilution , 1992, Biology and Fertility of Soils.

[48]  P. Curtis,et al.  Soil Microbial Communities Beneath Populus Grandidentata Grown Under Elevated Atmospheric CO2 , 1996 .

[49]  J. Aber,et al.  Factors controlling atmospheric methane consumption by temperate forest soils , 1995 .

[50]  R. Atlas,et al.  Microbial Ecology: Fundamentals and Applications. , 1982 .

[51]  G. Berntson,et al.  Nitrogen cycling in microcosms of yellow birch exposed to elevated CO2: simultaneous positive and negative below‐ground feedbacks , 1997 .

[52]  G. Hendrey.  FACE: Free-Air CO{sub 2} Enrichment for plant research in the field , 1992 .

[53]  R. Phillips,et al.  Influence of atmospheric CO2 enrichment on methane consumption in a temperate forest soil , 2001 .

[54]  L. Bakken,et al.  N2O and CH4 fluxes in soil influenced by fertilization and tractor traffic , 1993 .

[55]  E. Rastetter,et al.  Nutrients: Dynamics and Limitations , 1999 .

[56]  W. Schlesinger.  Biogeochemistry: An Analysis of Global Change , 1991 .

[57]  D. Binkley,et al.  Ecology and Management of Forest Soils , 2000 .

[58]  R. Knowles,et al.  Atmospheric Methane Consumption by Forest Soils and Extracted Bacteria at Different pH Values , 1998, Applied and Environmental Microbiology.

[59]  S. Zechmeister-Boltenstern,et al.  Oxidation of ethylene and methane in forest soils—effect of CO2 and mineral nitrogen , 1999 .

[60]  K. A. Sandbeck,et al.  Rapid Methane Oxidation in a Landfill Cover Soil , 1990, Applied and environmental microbiology.

[61]  J. Melillo,et al.  Soil moisture as a predictor of methane uptake by temperate forest soils , 1994 .

[62]  M. Rillig,et al.  Below-ground microbial and microfaunal responses to Artemisia tridentata grown under elevated atmospheric CO2 , 1996 .

[63]  Michael J. Whiticar,et al.  Biogenic methane formation in marine and freshwater environments: CO2 reduction vs. acetate fermentation—Isotope evidence , 1986 .

[64]  W. Schlesinger,et al.  Effects of elevated atmospheric CO2 on fine root production and activity in an intact temperate forest ecosystem , 2000 .

[65]  Reinhart Ceulemans,et al.  Tansley Review No. 71 Effects of elevated atmospheric CO2on woody plants , 1994 .

[66]  W. Cheng.  9 – Rhizosphere Processes under Elevated CO2 , 1999 .

[67]  Eugene W. Nester,et al.  Microbiology: A Human Perspective , 1995 .

[68]  M. Press,et al.  Elevated concentrations of CO2 may double methane emissions from mires , 1995 .

[69]  H. Weigel,et al.  Effects of CO2 enrichment and intraspecific competition on biomass partitioning, nitrogen content and microbial biomass carbon in soil of perennial ryegrass and white clover , 1995 .

[70]  D. Ellsworth,et al.  Tree and forest functioning in an enriched CO2 atmosphere , 1998 .

[71]  E. Pattey,et al.  Soils as sources and sinks for atmospheric methane. , 1997 .

[72]  M. Bender,et al.  Effect of CH4 concentrations and soil conditions on the induction of CH4 oxidation activity , 1995 .

[73]  G. Katul,et al.  A Lagrangian dispersion model for predicting CO2 sources, sinks, and fluxes in a uniform loblolly pine (Pinus taeda L.) stand , 1997 .

[74]  T. A. Kursar,et al.  The effects of the rainy season and irrigation on soil water and oxygen in a seasonal forest in Panama , 1995, Journal of Tropical Ecology.

[75]  Graham D. Farquhar,et al.  An Empirical Model of Stomatal Conductance , 1984 .

[76]  P. Ambus,et al.  Fluxes of CH4 and N2O in aspen stands grown under ambient and twice-ambient CO2 , 1999, Plant and Soil.

[77]  George R. Hendrey,et al.  The FACE program , 1994 .

[78]  W. Schlesinger,et al.  EFFECTS OF FREE-AIR CO2 ENRICHMENT (FACE) ON BELOWGROUND PROCESSES IN A PINUS TAEDA FOREST , 2000 .

[79]  G. Hendrey,et al.  Microbial community changes in the rhizospheres of white clover and perennial ryegrass exposed to free air carbon dioxide enrichment (FACE) , 1996 .

[80]  P. Curtis,et al.  Elevated atmospheric CO2 and feedback between carbon and nitrogen cycles , 1993, Plant and Soil.

[81]  H. Rouhier,et al.  Carbon fluxes in the rhizosphere of sweet chestnut seedlings (Castanea sativa) grown under two atmospheric CO2 concentrations: 14C partitioning after pulse labelling , 1996, Plant and Soil.

[82]  A. Ball,et al.  The decomposition of Lolium perenne in soils exposed to elevated CO2: comparisons of mass loss of litter with soil respiration and soil microbial biomass , 2000 .

[83]  Response of plants to CO2 under water limited conditions , 1993 .

[84]  R. B. Jackson,et al.  CO2 alters water use, carbon gain, and yield for the dominant species in a natural grassland , 1994, Oecologia.

[85]  J. Amthor.  Increasing Atmospheric CO2 Concentration, Water Use, and Water Stress: Scaling Up from the Plant to the Landscape , 1999 .

[86]  G. King,et al.  Survival and Recovery of Methanotrophic Bacteria Starved under Oxic and Anoxic Conditions , 1994, Applied and environmental microbiology.

[87]  W. Larcher.  Physiological Plant Ecology , 1977 .

[88]  Tim R. Moore,et al.  THE INFLUENCE OF WATER TABLE LEVELS ON METHANE AND CARBON DIOXIDE EMISSIONS FROM PEATLAND SOILS , 1989 .

[89]  W. Reeburgh,et al.  Oxidation of methane in boreal forest soils: a comparison of seven measures , 1992 .

[90]  R. Striegl.  Diffusional limits to the consumption of atmospheric methane by soils , 1993 .

[91]  H. Rogers,et al.  Effects of free-air CO2 enrichment on microbial populations in the rhizosphere and phyllosphere of cotton , 1994 .

[92]  H. Gholz,et al.  Effects of forest harvesting on soil methane fluxes in Florida slash pine plantations , 2000 .

[93]  G. King,et al.  Responses of methanotrophic activity in soils and cultures to water stress , 1996, Applied and environmental microbiology.

[94]  B. Drake,et al.  Stimulation of methane emission by carbon dioxide enrichment of marsh vegetation , 1994, Nature.

[95]  P. Ineson,et al.  Soil gas fluxes of N2O, CH4 and CO2 beneath Lolium perenne under elevated CO2: The Swiss free air carbon dioxide enrichment experiment , 2004, Plant and Soil.

[96]  C. Körner,et al.  Soil moisture dynamics of calcareous grassland under elevated CO2 , 1998, Oecologia.

[97]  G. Katul,et al.  Hydrologic balance in an intact temperate forest ecosystem under ambient and elevated atmospheric CO2 concentration , 2002 .

[98]  W. Schlesinger,et al.  Soil CO2 dynamics, acidification, and chemical weathering in a temperate forest with experimental CO2 enrichment , 2001 .

[99]  D. Ellsworth,et al.  Forest litter production, chemistry and decomposition following two years of Free-Air CO2 Enrichment , 2001 .