, Volume 95, Issue 1, pp 37–59 | Cite as

Biological and physical influences on the carbon isotope content of CO2 in a subalpine forest snowpack, Niwot Ridge, Colorado

  • D. R. BowlingEmail author
  • W. J. Massman
  • S. M. Schaeffer
  • S. P. Burns
  • R. K. Monson
  • M. W. Williams
Original Paper


Considerable research has recently been devoted to understanding biogeochemical processes under winter snow cover, leading to enhanced appreciation of the importance of many winter ecological processes. In this study, a comprehensive investigation of the stable carbon isotope composition (δ13C) of CO2 within a high-elevation subalpine forest snowpack was conducted. Our goals were to study the δ13C of biological soil respiration under snow in winter, and to assess the relative importance of diffusion and advection (ventilation by wind) for gas transport within snow. In agreement with other studies, we found evidence of an active microbial community under a roughly 1-m deep snowpack during winter and into spring as it melted. Under-snow CO2 mole fractions were observed up to 3,500 μmol mol−1, and δ13C of CO2 varied from ~−22 to ~−8‰. The δ13C of soil respiration calculated from mixing relationships was −26 to −24‰, and although it varied in time, it was generally close to that of the bulk organic horizon (−26.0‰). Subnivean CO2 and δ13C were quite dynamic in response to changes in soil temperature, liquid water availability, and wind events. No clear biologically-induced isotopic changes were observed during periods when microbial activity and root/rhizosphere activity were expected to vary, although such changes cannot be eliminated. There was clear evidence of isotopic enrichment associated with diffusive transport as predicted by theory, but simple diffusive enrichment (4.4‰) was not observed. Instead, ventilation of the snowpack by sustained wind events in the forest canopy led to changes in the diffusively-enriched gas profile. The isotopic influence of diffusion on gases in the snowpack and litter was greatest at greater depths, due to the decreased relative contribution of advection at depth. There were highly significant correlations between the apparent isotopic content of respiration from the soil with wind speed and pressure. In summary, physical factors influencing gas transport substantially modified and potentially obscured biological factors in their effects on δ13C of CO2 within this subalpine forest snowpack.


Carbon dioxide Microbial Niwot Ridge AmeriFlux site Soil respiration Stable isotope Winter 



Data from this project are available for collaborative use by anyone interested—contact the senior author. Kurt Chowanski, Lucas Zukiewicz, and Dave Millar of the University of Colorado Mountain Research Station and Niwot Ridge Long-Term Ecological Research (LTER) project helped maintain the TDL in the field, and these folks plus Ken Hill and Scott Jackson dug the snow pits. Thanks to Sarah Gaines and Andy Schauer for preparation and measurement of calibration gases at the Stable Isotope Ratio Facility for Environmental Research at the University of Utah, and to Chris Landry of the Center for Snow and Avalanche Studies and Bert Tanner of Campbell Scientific for helpful discussions regarding snow temperature measurement. We thank Paul Brooks, Thure Cerling, and Andrew Moyes for helpful discussions and comments on an early draft. We are grateful to the USDA Natural Resources Conservation Service, Colorado Snow Survey Program for maintaining the SNOTEL network and freely sharing their data for this study. This research was supported by a grant to DRB from the Office of Science (BER), U. S. Department of Energy, Grant No. DE-FG02-04ER63904. We acknowledge the additional support of a grant from the National Institute for Climate Change Research (NICCR) Western Section to RKM, and National Science Foundation grant DEB 0423662 to the Niwot Ridge LTER program.


  1. Aitchison CW (2001) The effect of snow cover on small animals. In: Jones HG, Pomeroy JW, Walker DA, Hoham RW (eds) Snow ecology: an interdisciplinary examination of snow-covered systems. Cambridge University Press, CambridgeGoogle Scholar
  2. Albert MR (2002) Effects of snow and firn ventilation on sublimation rates. Ann Glaciol 35:52–56. doi: 10.3189/172756402781817194 CrossRefGoogle Scholar
  3. Albert MR, Hardy JP (1995) Ventilation experiments in a seasonal snow cover. In: Tonnessen KA, Williams MA, Tranter M (eds) Biogeochemistry of seasonally snow-covered catchments. International Association of Hydrologic Sciences Press, Institute of Hydrology, Wallingford, pp 41–49Google Scholar
  4. Albert MR, Shultz EF (2002) Snow and firn properties and air-snow transport processes at Summit, Greenland. Atmos Environ 36:2789–2797. doi: 10.1016/S1352-2310(02)00119-X CrossRefGoogle Scholar
  5. Alstad KP, Lai C-T, Flanagan LB, Ehleringer JR (2007) Environmental controls on the carbon isotope composition of ecosystem-respired CO2 in contrasting forest ecosystems in Canada and the USA. Tree Physiol 27:1361–1374Google Scholar
  6. Amundson R, Stern L, Baisden T, Wang Y (1998) The isotopic composition of soil and soil-respired CO2. Geoderma 82:83–114. doi: 10.1016/S0016-7061(97)00098-0 CrossRefGoogle Scholar
  7. Anthoni PM, Law BE, Unsworth MH (1999) Carbon and water vapor exchange of an open-canopied ponderosa pine ecosystem. Agric For Meteorol 95:151–168. doi: 10.1016/S0168-1923(99)00029-5 CrossRefGoogle Scholar
  8. Assonov SS, Brenninkmeijer CAM, Jockel P (2005) The 18O isotope exchange rate between firn air CO2 and the firn matrix at three Antarctic sites. J Geophys Res 110:D18310. doi: 18310.11029/12005JD005769 CrossRefGoogle Scholar
  9. Böstrom B, Comstedt D, Ekblad A (2007) Can isotopic fractionation during respiration explain the 13C-enriched sporocarps of ectomycorrhizal and saprotrophic fungi? New Phytol 177:1012–1019. doi: 10.1111/j.1469-8137.2007.02332.x CrossRefGoogle Scholar
  10. Bowling DR, McDowell NG, Bond BJ, Law BE, Ehleringer JR (2002) 13C content of ecosystem respiration is linked to precipitation and vapor pressure deficit. Oecologia 131:113–124. doi: 10.1007/s00442-001-0851-y CrossRefGoogle Scholar
  11. Bowling DR, Burns SP, Conway TJ, Monson RK, White JWC (2005) Extensive observations of CO2 carbon isotope content in and above a high-elevation subalpine forest. Global Biogeochem Cycles 19:GB3023. doi: 3010.1029/2004GB002394 CrossRefGoogle Scholar
  12. Bowling DR, Pataki DE, Randerson JT (2008) Carbon isotopes in terrestrial ecosystem pools and CO2 fluxes. New Phytol 178:24–40. doi: 10.1111/j.1469-8137.2007.02342.x CrossRefGoogle Scholar
  13. Brooks PD, Williams MW, Schmidt SK (1996) Microbial activity under alpine snowpacks, Niwot Ridge, Colorado. Biogeochemistry 32:93–113. doi: 10.1007/BF00000354 CrossRefGoogle Scholar
  14. Brooks PD, Schmidt SK, Williams MW (1997) Winter production of CO2 and N2O from alpine tundra: environmental controls and relationship to inter-system C and N fluxes. Oecologia 110:403–413Google Scholar
  15. Brooks PD, McKnight D, Elder K (2005) Carbon limitation of soil respiration under winter snowpacks: potential feedbacks between growing season and winter carbon fluxes. Glob Change Biol 11:231–238. doi: 10.1111/j.1365-2486.2004.00877.x CrossRefGoogle Scholar
  16. Cerling TE, Solomon DK, Quade J, Bowman JR (1991) On the isotopic composition of carbon in soil carbon dioxide. Geochim Cosmochim Acta 55:3403–3405. doi: 10.1016/0016-7037(91)90498-T CrossRefGoogle Scholar
  17. Chen BZ, Chen JM, Huang L, Tans PP (2006) Modeling dynamics of stable carbon isotopic exchange between a boreal forest ecosystem and the atmosphere. Glob Change Biol 12:1842–1867. doi: 10.1111/j.1365-2486.2006.01200.x CrossRefGoogle Scholar
  18. Clark ID, Henderson L, Chappellaz J, Fisher D, Koerner R, Worthy DEJ, Kotzer T, Norman AL, Barnola JM (2007) CO2 isotopes as tracers of firn air diffusion and age in an Arctic ice cap with summer melting, Devon Island, Canada. J Geophys Res 112:D01301. doi: 01310.01029/02006JD007471 CrossRefGoogle Scholar
  19. Coxson DS, Parkinson D (1987) Winter respiratory activity in aspen woodland forest floor litter and soils. Soil Biol Biochem 19:49–59. doi: 10.1016/0038-0717(87)90125-8 CrossRefGoogle Scholar
  20. Davidson GR (1995) The stable isotopic composition and measurement of carbon in soil CO2. Geochim Cosmochim Acta 59:2485–2489. doi: 10.1016/0016-7037(95)00143-3 CrossRefGoogle Scholar
  21. Edwards AC, Cresser MS (1992) Freezing and its effect on chemical and biological properties of soil. Adv Soil Sci 18:59–79Google Scholar
  22. Ekblad A, Högberg P (2001) Natural abundance of 13C in CO2 respired from forest soils reveals speed of link between tree photosynthesis and root respiration. Oecologia 127:305–308. doi: 10.1007/s004420100667 CrossRefGoogle Scholar
  23. Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 40:503–537. doi: 10.1146/annurev.pp.40.060189.002443 CrossRefGoogle Scholar
  24. Fernandez I, Mahieu N, Cadisch G (2003) Carbon isotopic fractionation during decomposition of plant materials of different quality. Global Biogeochem Cycles 17:1075. doi: 1010.1029/2001GB001834 CrossRefGoogle Scholar
  25. Flanagan LB, Brooks JR, Varney GT, Berry SC, Ehleringer JR (1996) Carbon isotope discrimination during photosynthesis and the isotope ratio of respired CO2 in boreal forest ecosystems. Global Biogeochem Cycles 10:629–640. doi: 10.1029/96GB02345 CrossRefGoogle Scholar
  26. Francey RJ, Allison CE, Etheridge DM, Trudinger CM, Enting IG, Leuenberger M et al (1999) A 1000-year high precision record of δ13C in atmospheric CO2. Tellus 51B:170–193Google Scholar
  27. Groffman PM, Hardy JP, Driscoll CT, Fahey TJ (2006) Snow depth, soil freezing, and fluxes of carbon dioxide, nitrous oxide and methane in a northern hardwood forest. Glob Change Biol 12:1748–1760. doi: 10.1111/j.1365-2486.2006.01194.x CrossRefGoogle Scholar
  28. Hardy JP, Davis RE, Winston GC (1995) Evolution of factors affecting gas transmissivity of snow in the boreal forest. In: Tonnessen KA, Williams MA, Tranter M (eds) Biogeochemistry of seasonally snow-covered catchments. International Association of Hydrologic Sciences Press, Institute of Hydrology, Wallingford, pp 51–59Google Scholar
  29. Hemming D, Yakir D, Ambus P, Aurela M, Besson C, Black K et al (2005) Pan-European δ13C values of air and organic matter from forest ecosystems. Glob Change Biol 11:1065–1093. doi: 10.1111/j.1365-2486.2005.00971.x CrossRefGoogle Scholar
  30. Hirano T (2005) Seasonal and diurnal variations in topsoil and subsoil respiration under snowpack in a temperate deciduous forest. Global Biogeochem Cycles 19:GB2011. doi: 2010.1029/2004GB002259 CrossRefGoogle Scholar
  31. Hoham RW, Duval B (2001) Microbial ecology of snow and freshwater ice with emphasis on snow algae. In: Jones HG, Pomeroy JW, Walker DA, Hoham RW (eds) Snow ecology: an interdisciplinary examination of snow-covered systems. Cambridge University Press, CambridgeGoogle Scholar
  32. Hood E, McKnight DM, Williams MW (2003) Sources and chemical character of dissolved organic carbon across an alpine/subalpine ecotone, Green Lakes Valley, Colorado Front Range, United States. Water Resour Res 39:1188. doi: 1110.1029/2002WR001738 CrossRefGoogle Scholar
  33. Keeling CD (1958) The concentration and isotopic abundances of atmospheric carbon dioxide in rural areas. Geochim Cosmochim Acta 13:322–334. doi: 10.1016/0016-7037(58)90033-4 CrossRefGoogle Scholar
  34. Kelley JJ, Weaver DF, Smith BP (1968) The variation of carbon dioxide under the snow in the Arctic. Ecology 49:358–361. doi: 10.2307/1934472 CrossRefGoogle Scholar
  35. Klumpp K, Schäufele R, Lötscher M, Lattanzi FA, Feneis W, Schnyder H (2005) C-isotope composition of CO2 respired by shoots and roots: fractionation during dark respiration? Plant Cell Environ 28:241–250. doi: 10.1111/j.1365-3040.2004.01268.x CrossRefGoogle Scholar
  36. Knohl A, Werner RA, Brand WA, Buchmann N (2005) Short-term variations in δ13C of ecosystem respiration reveals link between assimilation and respiration in a deciduous forest. Oecologia 142:70–82. doi: 10.1007/s00442-004-1702-4 CrossRefGoogle Scholar
  37. Kueppers LM, Harte J (2005) Subalpine forest carbon cycling: short- and long-term influence of climate and species. Ecol Appl 15:1984–1999. doi: 10.1890/04-1769 CrossRefGoogle Scholar
  38. Lai C-T, Ehleringer JR, Schauer AJ, Tans PP, Hollinger DY, Paw UKT et al (2005) Canopy-scale δ13C of photosynthetic and respiratory CO2 fluxes: observations in forest biomes across the United States. Glob Change Biol 11:633–643. doi: 10.1111/j.1365-2486.2005.00931.x CrossRefGoogle Scholar
  39. Lewicki JL, Evans WC, Hilley GE, Sorey ML, Rogie JD, Brantley SL (2003) Shallow soil CO2 flow along the San Andreas and Calaveras Faults, California. J Geophys Res 108:2187. doi: 2110.1029/2002JB002141 CrossRefGoogle Scholar
  40. Lipson DA (2007) Relationships between temperature responses and bacterial community structure along seasonal and altitudinal gradients. FEMS Microbiol Ecol 59:418–427. doi: 10.1111/j.1574-6941.2006.00240.x CrossRefGoogle Scholar
  41. Lipson DA, Monson RK (1998) Plant-microbe competition for soil amino acids in the alpine tundra: effects of freeze-thaw and dry-rewet events. Oecologia 113:406–414. doi: 10.1007/s004420050393 CrossRefGoogle Scholar
  42. Lipson DA, Schmidt SK, Monson RK (2000) Carbon availability and temperature control the post-snowmelt decline in alpine soil microbial biomass. Soil Biol Biochem 32:441–448. doi: 10.1016/S0038-0717(99)00068-1 CrossRefGoogle Scholar
  43. Mariko S, Nishimura N, Mo WH, Matsui Y, Kibe T, Koizumi H (2000) Winter CO2 flux from soil and snow surfaces in a cool-temperate deciduous forest, Japan. Ecol Res 15:363–372. doi: 10.1046/j.1440-1703.2000.00357.x CrossRefGoogle Scholar
  44. Massman WJ (2006) Advective transport of CO2 in permeable media induced by atmospheric pressure fluctuations: 1. An analytical model. J Geophys Res 111:G03004. doi: 03010.01029/02006JG000163 CrossRefGoogle Scholar
  45. Massman WJ, Frank JM (2006) Advective transport of CO2 in permeable media induced by atmospheric pressure fluctuations: 2. Observational evidence under snowpacks. J Geophys Res 111:G03005. doi: 03010.01029/02006JG000164 CrossRefGoogle Scholar
  46. Massman WJ, Sommerfeld RA, Mosier AR, Zeller KF, Hehn TJ, Rochelle SG (1997) A model investigation of turbulence-driven pressure-pumping effects on the rate of diffusion of CO2, N2O, and CH4 through layered snowpacks. J Geophys Res 102:18851–18863. doi: 10.1029/97JD00844 CrossRefGoogle Scholar
  47. Mast MA, Wickland KP, Striegl RT, Clow DW (1998) Winter fluxes of CO2 and CH4 from subalpine soils in Rocky Mountain National Park, Colorado. Global Biogeochem Cycles 12:607–620. doi: 10.1029/98GB02313 CrossRefGoogle Scholar
  48. Matzner E, Borken W (2008) Do freeze-thaw events enhance C and N losses from soils of different ecosystems? A review. Eur J Soil Sci 59:274–284. doi: 10.1111/j.1365-2389.2007.00992.x CrossRefGoogle Scholar
  49. McDowell NG, Marshall JD, Hooker TD, Musselman R (2000) Estimating CO2 flux from snowpacks at three sites in the Rocky Mountains. Tree Physiol 20:745–753Google Scholar
  50. McDowell NG, Bowling DR, Schauer A, Irvine J, Bond BJ, Law BE et al (2004) Associations between carbon isotope ratios of ecosystem respiration, water availability and canopy conductance. Glob Change Biol 10:1767–1784. doi: 10.1111/j.1365-2486.2004.00837.x CrossRefGoogle Scholar
  51. Mikan CJ, Schimel JP, Doyle AP (2002) Temperature controls of microbial respiration in arctic tundra soils above and below freezing. Soil Biol Biochem 34:1785–1795. doi: 10.1016/S0038-0717(02)00168-2 CrossRefGoogle Scholar
  52. Monson RK, Turnipseed AA, Sparks JP, Harley PC, Scott-Denton LE, Sparks K et al (2002) Carbon sequestration in a high-elevation, subalpine forest. Glob Change Biol 8:459–478. doi: 10.1046/j.1365-2486.2002.00480.x CrossRefGoogle Scholar
  53. Monson RK, Sparks JP, Rosenstiel TN, Scott-Denton LE, Huxman TE, Harley PC et al (2005) Climatic influences on net ecosystem CO2 exchange during the transition from wintertime carbon source to springtime carbon sink in a high-elevation, subalpine forest. Oecologia 146:130–147. doi: 10.1007/s00442-005-0169-2 CrossRefGoogle Scholar
  54. Monson RK, Burns SP, Williams MW, Delany AC, Weintraub M, Lipson DA (2006a) The contribution of beneath-snow soil respiration to total ecosystem respiration in a high-elevation, subalpine forest. Global Biogeochem Cycles 20:GB3030. doi: 3010.1029/2005GB002684 CrossRefGoogle Scholar
  55. Monson RK, Lipson DL, Burns SP, Turnipseed AA, Delany AC, Williams MW et al (2006b) Winter forest soil respiration controlled by climate and microbial community composition. Nature 439:711–714. doi: 10.1038/nature04555 CrossRefGoogle Scholar
  56. Mortazavi B, Chanton JP, Prater JL, Oishi AC, Oren R, Katul G (2005) Temporal variability in 13C of respired CO2 in a pine and a hardwood forest subject to similar climatic conditions. Oecologia 142:57–69. doi: 10.1007/s00442-004-1692-2 CrossRefGoogle Scholar
  57. Murayama S, Saigusa N, Chan D, Yamamoto S, Kondo H, Eguchi Y (2003) Temporal variations of atmospheric CO2 concentration in a temperate deciduous forest in central Japan. Tellus B Chem Phys Meterol 55:232–243. doi: 10.1034/j.1600-0889.2003.00061.x CrossRefGoogle Scholar
  58. Musselman RC, Massman WJ, Frank JM, Korfmacher JL (2005) The temporal dynamics of carbon dioxide under snow in a high elevation Rocky Mountain subalpine forest and meadow. Arct Antarct Alp Res 37:527–538. doi: 10.1657/1523-0430(2005)037[0527:TTDOCD]2.0.CO;2 CrossRefGoogle Scholar
  59. Nobel PS (2005) Physicochemical and environmental plant physiology. Elsevier Academic Press, AmsterdamGoogle Scholar
  60. Oechel WC, Vourlitis G, Hastings SJ (1997) Cold season CO2 emission from arctic soils. Global Biogeochem Cycles 11:163–172. doi: 10.1029/96GB03035 CrossRefGoogle Scholar
  61. Panikov NS, Flanagan PW, Oechel WC, Mastepanov MA, Christensen TR (2006) Microbial activity in soils frozen to below −39 degrees C. Soil Biol Biochem 38:785–794. doi: 10.1016/j.soilbio.2005.07.004 CrossRefGoogle Scholar
  62. Pataki DE, Ehleringer JR, Flanagan LB, Yakir D, Bowling DR, Still CJ, Buchmann N, Kaplan JO, Berry JA (2003) The application and interpretation of Keeling plots in terrestrial carbon cycle research. Global Biogeochem Cycles 17:1022. doi: 1010.1029/2001GB001850 CrossRefGoogle Scholar
  63. Ponton S, Flanagan LB, Alstad KP, Johnson BG, Morgenstern K, Kljun N et al (2006) Comparison of ecosystem water-use efficiency among Douglas-fir forest, aspen forest and grassland using eddy covariance and carbon isotope techniques. Glob Change Biol 12:294–310. doi: 10.1111/j.1365-2486.2005.01103.x CrossRefGoogle Scholar
  64. Randerson JT, Collatz GJ, Fessenden JE, Munoz AD, Still CJ, Berry JA, Fung IY, Suits N, Denning AS (2002) A possible global covariance between terrestrial gross primary production and 13C discrimination: consequences for the atmospheric 13C budget and its response to ENSO. Global Biogeochem Cycles 16:1136. doi: 1110.1029/2001GB001845 CrossRefGoogle Scholar
  65. Sacks WJ, Schimel DS, Monson RK (2007) Coupling between carbon cycling and climate in a high-elevation, subalpine forest: a model-data fusion analysis. Oecologia 151:54–58. doi: 10.1007/s00442-006-0565-2 CrossRefGoogle Scholar
  66. Schadt CW, Martin AP, Lipson DA, Schmidt SK (2003) Seasonal dynamics of previously unknown fungal lineages in tundra soils. Science 301:1359–1361. doi: 10.1126/science.1086940 CrossRefGoogle Scholar
  67. Schaeffer SM, Anderson DE, Burns SP, Monson RK, Sun J, Bowling DR (2008) Canopy structure and atmospheric flows in relation to the δ13C of respired CO2 in a subalpine coniferous forest. Agric For Meteorol 148:592–605. doi: 10.1016/j.agrformet.2007.11.003 CrossRefGoogle Scholar
  68. Schaeffer SM, Miller JB, Vaughn BH, White JWC & Bowling DR (in press) Long-term field performance of a tunable diode laser absorption spectrometer for analysis of carbon isotopes of CO2 in forest air. Atmos Chem PhysGoogle Scholar
  69. Schimel JP, Clein JS (1996) Microbial response to freeze-thaw cycles in tundra and taiga soils. Soil Biol Biochem 28:1061–1066. doi: 10.1016/0038-0717(96)00083-1 CrossRefGoogle Scholar
  70. Schindlbacher A, Zechmeister-Boltenstern S, Glatzel G, Jandl R (2007) Winter soil respiration from an Austrian mountain forest. Agric For Meteorol 146:205–215. doi: 10.1016/j.agrformet.2007.06.001 CrossRefGoogle Scholar
  71. Schmidt SK, Lipson DA (2004) Microbial growth under the snow: implications for nutrient and allelochemical availability in temperate soils. Plant Soil 259:1–7. doi: 10.1023/B:PLSO.0000020933.32473.7e CrossRefGoogle Scholar
  72. Schmidt SK, Wilson KL, Meyer AF, Gebauer MM, King AJ (2008) Phylogeny and ecophysiology of opportunistic “snow molds” from a subalpine forest ecosystem. Microb Ecol. doi: 10.1007/s00248-00008-09387-00246
  73. Schmidt SK, Wilson KL, Monson RK, Lipson DA (in review (part of the White on Green special issue)) Exponential growth of “snow molds” at sub-zero temperatures: an explanation for high beneath-snow respiration rates and Q10 values. BiogeochemistryGoogle Scholar
  74. Schnyder H, Lattanzi FA (2005) Partitioning respiration of C3–C4 mixed communities using the natural abundance 13C approach – testing assumptions in a controlled environment. Plant Biol 7:592–600. doi: 10.1055/s-2005-872872 CrossRefGoogle Scholar
  75. Scholze M, Ciais P, Heimann M (2008) Modeling terrestrial 13C cycling: climate, land use and fire. Global Biogeochem Cycles 22:GB1009. doi: 1010.1029/2006GB002899 CrossRefGoogle Scholar
  76. Scott-Denton LE, Rosenstiel TN, Monson RK (2006) Differential controls by climate and substrate over the heterotrophic and rhizospheric components of soil respiration. Glob Change Biol 12:205–216. doi: 10.1111/j.1365-2486.2005.01064.x CrossRefGoogle Scholar
  77. Solomon DK, Cerling TE (1987) The annual carbon dioxide cycle in a montane soil: observations, modeling, and implications for weathering. Water Resour Res 23:2257–2265. doi: 10.1029/WR023i012p02257 CrossRefGoogle Scholar
  78. Sommerfeld RA, Musselman RC, Reuss JO, Mosier AR (1991) Preliminary measurements of CO2 in melting snow. Geophys Res Lett 18:1225–1228. doi: 10.1029/91GL01502 CrossRefGoogle Scholar
  79. Sommerfeld RA, Mosier AR, Musselman RC (1993) CO2, CH4 and N2O flux through a Wyoming snowpack and implications for global budgets. Nature 361:140–142. doi: 10.1038/361140a0 CrossRefGoogle Scholar
  80. Sturm M, Johnson JB (1991) Natural convection in the subarctic snow cover. J Geophys Res 96:11657–11671. doi: 10.1029/91JB00895 CrossRefGoogle Scholar
  81. Suits NS, Denning AS, Berry JA, Still CJ, Kaduk J, Miller JB, Baker IT (2005) Simulation of carbon isotope discrimination of the terrestrial biosphere. Global Biogeochem Cycles 19:GB1017. doi: 1010.1029/2003GB002141 CrossRefGoogle Scholar
  82. Suni T, Berninger F, Vesala T, Markkanen T, Hari P, Makela A et al (2003) Air temperature triggers the recovery of evergreen boreal forest photosynthesis in spring. Glob Change Biol 9:1410–1426. doi: 10.1046/j.1365-2486.2003.00597.x CrossRefGoogle Scholar
  83. Suzuki S, Ishizuka S, Kitamura K, Yamanoi K, Nakai Y (2006) Continuous estimation of winter carbon dioxide efflux from the snow surface in a deciduous broadleaf forest. J Geophys Res 111:D17101. doi: 17110.11029/12005JD006595 CrossRefGoogle Scholar
  84. Takagi K, Nomura M, Ashiya D, Takahashi H, Sasa K, Fujinuma Y, Shibata H, Akibayashi Y, Koike T (2005) Dynamic carbon dioxide exchange through snowpack by wind-driven mass transfer in a conifer-broadleaf mixed forest in northernmost Japan. Global Biogeochem Cycles 19:GB2012. doi: 2010.1029/2004GB002272 CrossRefGoogle Scholar
  85. Trudinger CM, Enting IG, Etheridge DM, Francey RJ, Levchenko VA, Steele LP et al (1997) Modeling air movement and bubble trapping in firn. J Geophys Res 102:6747–6763. doi: 10.1029/96JD03382 CrossRefGoogle Scholar
  86. Uchida M, Mo W, Nakatsubo T, Tsuchiya Y, Horikoshi T, Koizumi H (2005) Microbial activity and litter decomposition under snow cover in a cool-temperate broad-leaved deciduous forest. Agric For Meteorol 134:102–109. doi: 10.1016/j.agrformet.2005.11.003 CrossRefGoogle Scholar
  87. Weintraub MN, Scott-Denton LE, Schmidt SK, Monson RK (2007) The effects of tree rhizodeposition on soil exoenzyme activity, dissolved organic carbon, and nutrient availability in a subalpine forest ecosystem. Oecologia 154:327–338. doi: 10.1007/s00442-007-0804-1 CrossRefGoogle Scholar
  88. Williams MW, Cline D, Hartman M, Bardsley T (1999) Data for snowmelt model development, calibration, and verification at an alpine site, Colorado Front Range. Water Resour Res 35:3205–3209. doi: 10.1029/1999WR900088 CrossRefGoogle Scholar
  89. Winston GC, Stephens BB, Sundquist ET, Hardy JP, Davis RE (1995) Seasonal variability in CO2 transport through snow in a boreal forest. In: Tonnessen KA, Williams MA, Tranter M (eds) Biogeochemistry of seasonally snow-covered catchments. International Association of Hydrologic Sciences Press, Institute of Hydrology, Wallingford, pp 61–70Google Scholar
  90. Zhang J, Quay PD, Wilbur DO (1995) Carbon isotope fractionation during gas-water exchange and dissolution of CO2. Geochim Cosmochim Acta 59:107–114. doi: 10.1016/0016-7037(95)91550-D CrossRefGoogle Scholar
  91. Zimov SA, Zimova GM, Daviodov SP, Daviodova AI, Voropaev YV, Voropaeva ZV et al (1993) Winter biotic activity and production of CO2 in Siberian soils: a factor in the greenhouse effect. J Geophys Res 98:5017–5023. doi: 10.1029/92JD02473 CrossRefGoogle Scholar
  92. Zobitz JM, Keener JP, Schnyder H, Bowling DR (2006) Sensitivity analysis and quantification of uncertainty for isotopic mixing relationships in carbon cycle research. Agric For Meteorol 136:56–75CrossRefGoogle Scholar
  93. Zobitz JM, Burns SP, Ogée J, Reichstein M, Bowling DR (2007) Partitioning net ecosystem exchange of CO2: a comparison of a Bayesian/isotope approach to environmental regression methods. J Geophys Res 112:G03013. doi: 03010.01029/02006JG000282 CrossRefGoogle Scholar
  94. Zobitz JM, Burns SP, Reichstein M, Bowling DR (2008) Partitioning net ecosystem carbon exchange and the carbon isotopic disequilibrium between whole-ecosystem photosynthesis and respiration in a subalpine forest. Glob Change Biol 14:1785–1800CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • D. R. Bowling
    • 1
    Email author
  • W. J. Massman
    • 2
  • S. M. Schaeffer
    • 1
    • 3
  • S. P. Burns
    • 4
    • 5
  • R. K. Monson
    • 6
    • 7
  • M. W. Williams
    • 8
  1. 1.Department of BiologyUniversity of UtahSalt Lake CityUSA
  2. 2.Rocky Mountain Research StationUSDA Forest ServiceFort CollinsUSA
  3. 3.Department of Ecology, Evolution, and Marine BiologyUniversity of CaliforniaSanta BarbaraUSA
  4. 4.Department of Ecology and Evolutionary BiologyUniversity of ColoradoBoulderUSA
  5. 5.National Center for Atmospheric ResearchBoulderUSA
  6. 6.Department of Ecology and Evolutionary BiologyUniversity of ColoradoBoulderUSA
  7. 7.Cooperative Institute for Research in Environmental SciencesUniversity of ColoradoBoulderUSA
  8. 8.Institute of Arctic and Alpine Research and Department of GeographyUniversity of ColoradoBoulderUSA

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