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Climatic influences on net ecosystem CO2 exchange during the transition from wintertime carbon source to springtime carbon sink in a high-elevation, subalpine forest

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Abstract

The transition between wintertime net carbon loss and springtime net carbon assimilation has an important role in controlling the annual rate of carbon uptake in coniferous forest ecosystems. We studied the contributions of springtime carbon assimilation to the total annual rate of carbon uptake and the processes involved in the winter-to-spring transition across a range of scales from ecosystem CO2 fluxes to chloroplast photochemistry in a coniferous, subalpine forest. We observed numerous initiations and reversals in the recovery of photosynthetic CO2 uptake during the initial phase of springtime recovery in response to the passage of alternating warm- and cold-weather systems. Full recovery of ecosystem carbon uptake, whereby the 24-h cumulative sum of NEE (NEEdaily) was consistently negative, did not occur until 3–4 weeks after the first signs of photosynthetic recovery. A key event that preceded full recovery was the occurrence of isothermality in the vertical profile of snow temperature across the snow pack; thus, providing consistent daytime percolation of melted snow water through the snow pack. Interannual variation in the cumulative annual NEE (NEEannual) was mostly explained by variation in NEE during the snow-melt period (NEEsnow-melt), not variation in NEE during the snow-free part of the growing season (NEEsnow-free). NEEsnow-melt was highest in those years when the snow melt occurred later in the spring, leading us to conclude that in this ecosystem, years with earlier springs are characterized by lower rates of NEEannual, a conclusion that contrasts with those from past studies in deciduous forest ecosystems. Using studies on isolated branches we showed that the recovery of photosynthesis occurred through a series of coordinated physiological and biochemical events. Increasing air temperatures initiated recovery through the upregulation of PSII electron transport caused in part by disengagement of thermal energy dissipation by the carotenoid, zeaxanthin. The availability of liquid water permitted a slightly slower recovery phase involving increased stomatal conductance. The most rate-limiting step in the recovery process was an increase in the capacity for the needles to use intercellular CO2, presumably due to slow recovery of Rubisco activity. Interspecific differences were observed in the timing of photosynthetic recovery for the dominant tree species. The results of our study provide (1) a context for springtime CO2 uptake within the broader perspective of the annual carbon budget in this subalpine forest, and (2) a mechanistic explanation across a range of scales for the coupling between springtime climate and the carbon cycle of high-elevation coniferous forest ecosystems.

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References

  • Adams WW, Demmig-Adams B (1992) Operation of the xanthophyll cycle in higher plants in response to diurnal changes in incident sunlight. Planta 189:390–398

    Google Scholar 

  • Adams WW, Demmig-Adams B, Rosenstiel TN, Ebbert V (2001) Dependence of photosynthesis and energy dissipation activity upon growth form and light environment during the winter. Photosyn Res 67:51–62

    Article  PubMed  CAS  Google Scholar 

  • Arain MA, Black TA, Barr AG, Jarvis PG, Massheder JM, Verseghy DL, Nesic Z (2002) Effects of seasonal and interannual climate variability on net ecosystem productivity of boreal deciduous and conifer forests. Can J For res 32:878–891

    Article  Google Scholar 

  • Baldocchi DD (2003) Assessing the eddy covariance technique for evaluating carbon dioxide exchange rates of ecosystems: past, present and future. Global Change Biol 9:479–492

    Article  Google Scholar 

  • Barr AG, Griffis TJ, Black TA, Lee X, Staebler RM, Fuentes JD, Chen Z, Morgenstern K (2002) Comparing the carbon budgets of boreal and temperate deciduous forest stands. Can J For Res 5:813–822

    Article  Google Scholar 

  • Bergh J, Linder S (1999) Effects of soil warming during spring on photosynthetic recovery in boreal Norway spruce stands. Global Change Biol 5:245–253

    Article  Google Scholar 

  • Bergh J, Freeman M, Sigurdsson B, Kellomaki S, Laitinen K, Niinisto S, Peltola H, Linder S (2003) Modelling the short-term effects of climate change on the productivity of selected tree species in Nordic countries. For Ecol Manag 183:327–340

    Article  Google Scholar 

  • Black TA, Chen WJ, Barr AG, Arain MA, Chen Z, Nesic Z, Hogg EH, Neumann HH, Yang PC (2000) Increased carbon sequestration by a boreal deciduous forest in years with a warm spring. Geophys Res Lett 27:1271–1274

    Article  Google Scholar 

  • Chen JM, Rich PM, Gower ST, Norman JM, Plummer S (1997) Leaf area index of boreal forests: Theory, techniques and measurements. J Geophys Res 102:29429–29443

    Article  Google Scholar 

  • Day TA, DeLucia EH, Smith WK (1989) Influence of cold soil and snowcover on photosynthesis and leaf conductance in two Rocky Mountain Conifers. Oecologia 80:546–552

    Article  Google Scholar 

  • DeLucia EH, Maherali H, Carey EV (2000) Climate-driven changes in biomass allocation in pines. Global Change Biol 6:587–593

    Article  Google Scholar 

  • Demmig-Adams B, Adams W, Barker DH, Logan BA, Verhoeven AS, Bowling DR (1996) Using chlorophyll fluorescence to assess the allocation of absorbed light to thermal dissipation of excess excitation. Physiol Plant 98:253–264

    Article  CAS  Google Scholar 

  • Ensminger I, Sveshnikov D, Campbell DA, Funk C, Jansson S, Lloyd J, Shibistova O, Oquist G (2004) Intermittent low temperatures constrain spring recovery of photosynthesis in boreal Scots pine forests. Global Change Biol 10:995–1008

    Article  Google Scholar 

  • Gilmore AM, Yamamoto HY (1991) Resolution of lutein and zexanthin using a nonendcapped, lightly carbon-loaded C18 high-performance liquid chromatographic column. J Chrom 543:137–145

    Article  CAS  Google Scholar 

  • Goulden ML, Munger JW, Fan S-M, Daube BC, Wofsy SC (1996a) Measurements of carbon sequestration by long-term eddy covariance: Methods and a critical evaluation of accuracy. Global Change Biol 2:169–182

    Article  Google Scholar 

  • Goulden ML, Munger JW, Fan S-M, Daube BC, Wofsy SC (1996b) CO2 exchange by a deciduous forest: response to interannual climate variability. Science 271:1576–1578

    Article  CAS  Google Scholar 

  • Hadley JL, Schedlbauer JL (2002) Carbon exchange of an old-growth eastern hemlock (Tsuga canadensis) forest in central New England. Tree Physiol 22:1079–1092

    PubMed  CAS  Google Scholar 

  • Harley PC, Thomas RB, Reynolds JF, Strain BR (1992) Modelling photosynthesis of cotton grown in elevated CO2. Plant, Cell & Environ 15:271–282

    Article  CAS  Google Scholar 

  • Huxman TE, Hamerlynck EP, Moore BD, Smith SD, Jordan DN, Zitzer SF, Nowak RS, Coleman J, Seemann JR (1998) Photosynthetic down-regulation in Larrea tridentata exposed to elevated atmospheric CO2: interaction with drought under glasshouse and field (FACE) exposure. Plant, Cell & Environ 21:1153–1161

    Article  Google Scholar 

  • Huxman TE, Turnipseed AA, Sparks JP, Harley PC, Monson RK (2003) Temperature as a control over ecosystem CO2 fluxes in a high-elevation, subalpine forest. Oecologia 134:537–546

    PubMed  CAS  Google Scholar 

  • Jacob J, Greitner C, Drake BG (1995) Acclimation of photosynthesis in relation to Rubisco and non-structural carbohydrate contents and in situ carboxylase activity in Scirpus olneyi grown at elevated CO2 in the field. Plant, Cell & Environ 18:875–884

    Article  CAS  Google Scholar 

  • Jurik TW, Briggs GM, Gates DM (1988) Springtime recovery of photosynthetic activity of white pine in Michigan. Can J Bot 66:138–141

    Google Scholar 

  • Kaimal JC, Finnigan JJ (1994) Atmospheric boundary layer flows: their structure and measurement. Oxford University Press, Oxford

    Google Scholar 

  • Law BE, Williams M, Anthoni PM, Baldocchi DD, Unsworth MH (2000) Measuring and modelling seasonal variation of carbon dioxide and water vapour exchange of a Pinus ponderosa forest subject to soil water deficit. Global Change Biol 6:613–630

    Article  Google Scholar 

  • Leverenz JW, Öquist G (1987) Quantum yields of photosynthesis at temperatures between 2 degrees and 35 degrees C in a cold-tolerant C3 plant (Pinus sylvestris) during the course of one year. Plant Cell Environ 10:287–295

    Article  Google Scholar 

  • Li S-P, Björkman O, Shih C, Grossman AR, Rosenquist M, Jansson S, Niyogi KK (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403:391–395

    Article  PubMed  CAS  Google Scholar 

  • Lloyd J, Langenfelds RL, Francey RJ, Gloor M, Tchebakova NM, Zolotoukhine D, Brand WA, Werner RA, Jordan A, Allison CA, Zrazhewske V, Shibistova O, Schulze ED (2002) A trace-gas climatology above Zotino, central Siberia. Tellus (Ser B) 54:749–767

    Article  Google Scholar 

  • Lundmark T, Bergh J, Strand M, Koppel A (1998) Seasonal variation of maximum photochemical efficiency in boreal Norway spruce stands. TREES-Struc Func 13:63–67

    Google Scholar 

  • Martinez-Vilalta J, Sala A, Pinol J (2004) The hydraulic architecture of Pinaceae-a review. Plant Ecol 171:3–13

    Article  Google Scholar 

  • Monson RK, Turnipseed AA, Sparks JP, Harley PC, Scott-Denton LE, Sparks K, Huxman TE (2002) Carbon sequestration in a high-elevation, subalpine forest. Global Change Biol 8:459–478

    Article  Google Scholar 

  • Myneni RB, Keeling CD, Tucker CJ, Asrar G, Nemani RR (1997) Increased plant growth in the northern high latitudes from 1981 to 1991. Nature 386:698–702

    Article  CAS  Google Scholar 

  • Nichol CJ, Lloyd J, Shibistova O, Arneth A, Roser C, Knohl A, Matsubara S, Grace J (2002) Remote sensing of photosynthetic-light-use efficiency of a Siberian boreal forest. Tellus (Ser B) 54:677–687

    Article  Google Scholar 

  • Öquist G, Huner NPA (2003) Photosynthesis of overwintering evergreen plants. Ann Rev Plant Biol 54:329–355

    Article  Google Scholar 

  • Ottander C, Öquist G (1991) Recovery of photosynthesis in winter-stressed Scots pine. Plant, Cell Environ 14:345–349

    Article  Google Scholar 

  • Pedhazur EJ (1997) Multiple regression in behavioral research, 3rd edn. Harcourt Brace College Publishers, New York

    Google Scholar 

  • Potvin C, Lechowicz MJ, Tardif S (1990) The statistical analysis of ecophysiological response curves obtained from experiments involving repeated measures. Ecology 71:1389–1400

    Article  Google Scholar 

  • Randerson JT, Field CB, Fung IY, Tans PP (1999) Increases in early season ecosystem uptake explain recent changes in the seasonal cycle of atmospheric CO2 at high northern latitudes. J Geophys Res 26:2765–2768

    CAS  Google Scholar 

  • Rebertus AJ, Burns BR, Veblen TT (1991) Stand dynamics of Pinus-flexilis-dominated sub-alpine forests in the Colorado Front Range. J Veg Sci 2:445–458

    Article  Google Scholar 

  • Smith WK (1985) Environmental limitations on leaf conductance in central Rocky Mountain conifers, USA. In: Turner H, Tranquillini W (eds) Establishment and tending of subalpine forest: research and management. Eidg Anst Forstl Versuchsw Ber 270, pp 95–101

    Google Scholar 

  • Smith NV, Saatchi SS, Randerson JT (2004) Trends in high northern latitude soil freeze and thaw cycles from 1988 to 2002. J Geophys Res 109:Art. No. D12101

    Google Scholar 

  • Suni T, Berninger F, Markkanen T, Keronen P, Rannik U, Vesala T (2003) Interannual variability and timing of growing-season CO2 exchange in a boreal forest. J Geophys Res 108(D9):Art No. 4265

    Article  Google Scholar 

  • Tanja S, Berninger F, Vesala T, Markkanen T, Hari P, Makela A, Ilvesniemi H, Hanninen H, Nikinmaa E, Huttula T, Laurila T, Aurela M, Grelle A, Lindroth A, Arneth A, Shibistova O, Lloyd J (2003) Air temperature triggers the recovery of evergreen boreal forest photosynthesis in spring. Global Change Biol 9:1410–1426

    Article  Google Scholar 

  • Troeng E, Linder S (1982) Gas-exchange in a 20-year old stand of Scots pine. 1. Net photosynthesis of current and one-year old shoots within and between seasons. Physiol Plant 54:7–14

    Article  CAS  Google Scholar 

  • Turnipseed AA, Blanken PD, Anderson DE, Monson RK (2002) Energy budget above a high-elevation subalpine forest in complex topography. Agric For Meteorol 110:177–201

    Article  Google Scholar 

  • Turnipseed AA, Anderson DE, Blanken PD, Baugh WM, Monson RK (2003) Airflows and turbulent flux measurements in mountainous terrain Part 1. Canopy and local effects. Agric For Meteorol 119:1–21

    Article  Google Scholar 

  • Turnipseed AA, Anderson DE, Blanken PD, Burns S, Monson RK (2004) Airflows and turbulent flux measurements in mountainous terrain Part 2. Mesoscale effects. Agric For Meteorol (in press)

  • Vaganov EA, Hughes MK, Kirdyanov AV, Schweingruber FH, Silkin PP (1999) Influence of snowfall and melt timing on tree growth in subarctic Eurasia. Nature 400:149–151

    Article  CAS  Google Scholar 

  • Verhoeven AS, Adams WW, Demmig-Adams B (1996) Close relationship between the state of the xanthophyll cycle pigments and photosystem II efficiency during recovery from winter stress. Physiol Plant 96:567–576

    Article  CAS  Google Scholar 

  • Verhoeven AS, Adams WW, Demmig-Adams B (1998) Two forms of sustained xanthophyll cycle-independent energy dissipation in overwintering Euonymus kiautchovicus. Plant Cell Environ 21:893–903

    Article  Google Scholar 

  • Verhoeven AS, Adams WW, Demmig-Adams B (1999) The xanthophyll cycle and acclimation of Pinus ponderosa and Malva neglecta to winter stress. Oecologia 118:277–287

    Article  Google Scholar 

  • Way J, Zimmermann R, Rignot E, McDonald K, Oren R (1997) Winter and spring thaw as observed with imaging radar at BOREAS. J Geophys Res 102:29673–29684

    Article  CAS  Google Scholar 

  • Webb EK, Pearman GI, Leuning R (1980) Correction of flux measurements for density effects due to heat and water vapor transfer. Quart J Roy Meteorol Soc 106:85–100

    Article  Google Scholar 

  • White MA, Running SW, Thornton PE (1999) The impact of growing-season length variability on carbon assimilation and evapotranspiration over 88 years in the eastern US deciduous forest. Intl J Biometeorol 42:139–145

    Article  Google Scholar 

  • Wilczak JM, Oncley SP, Stage SA (2001) Sonic anemometer tilt correction algorithms. Bound Lay Meteor 99:127–150

    Article  Google Scholar 

  • Yamazaki J, Ohashi A, Hashimoto Y, Negishi E, Kumagai S, Kubo T, Oikawa T, Maruta E, Kamimura Y (2003) Effects of high light and low temperature during harsh winter on needle photodamage of Abies mariesii growing at the forest limit on Mt. Norikura in Central Japan. Plant Sci 165:257–264

    Article  CAS  Google Scholar 

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Acknowledgements

We are grateful for the research contributions of many students and colleagues, including Kimberley Sparks, Bill Baugh, Dr. Chuixiang Yi, Sarah Schliemann, Andy McNown, Nathan Monson, Greg Monson, John Munch, Thomas Zukowski, and Wumesh Khatri. We are grateful to Mark Williams, Mark Loesleben and Andy O’Reilly who provided valuable guidance to making the snow temperature measurements. We thank Dr. Bill Bowman (University of Colorado Mountain Research Station) for providing valued logistical support in establishing and maintaining the Niwot Ridge AmeriFlux site and access to an additional gas exchange system. We thank Gordon Maclean and Tony Delany (National Center for Atmospheric Research) for their long-standing commitment to help with all types of technical issues surrounding the instrumentation at the Niwot Ridge AmeriFlux tower. We thank Dr. William Adams and Barbara Demmig-Adams for providing valuable access to the HPLC system used in the pigment analysis and to the chlorophyll fluorescence system used in the first recovery experiment. This work was financially supported by a grant from the South Central Section of the National Institute for Global Environmental Change (NIGEC) through the US Department of Energy (BER Program) (Cooperative Agreement No. DE-FC03-90ER61010). Any opinions, findings and conclusions or recommendations expressed in this publication are those of the authors and do not necessarily reflect the views of the DOE.

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Correspondence to Russell K. Monson.

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Communicated by Jim Ehleringer

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Monson, R.K., Sparks, J.P., Rosenstiel, T.N. et al. 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 (2005). https://doi.org/10.1007/s00442-005-0169-2

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