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Increased carbon sequestration by a boreal deciduous forest in years with a warm spring Barr, Alan G.; Chen, W. J.; Black, T. Andrew; Hogg, Edward H.; Nesic, Zoran; Yang, P. C.; Neumann, H. H.; Chen, Z.; Arain, M. Altaf May 31, 2000

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GEOPHYSICAL RESEARCH LETTERS, VOL. 27, NO. 9, PAGES 1271-1274, MAY 1, 2000  Increased carbon sequestration by a boreal forest in years with a warm spring  deciduous  T.A. Black,• W.J. Chen,•'2 A.G. Barr,a M.A. Arain,• Z. Chen,• Z . Nesic ,1 E.H. Hogg, 4 H.H. Neumann s andP.C. Yang• Abstract. A boreal deciduous forest in Saskatchewan, Canada, sequestered144i65, 80i60, 116-t-35 and 290-t-50 g  Prince Albert National Park, Saskatchewan, Canada. This mature aspen forest was regenerated after a natural fire iv_  C m-2 y-• in 1994,1996,1997and 1998,respectively. The  1919 [Weir, 1996], and in 1998 had a mean height of 21.5  increasedcarbon sequestrationwas the result of a warmer spring and earlier leaf emergence, which significantly increased ecosystemphotosynthesis,but had little effect on respiration. The high carbon sequestration in 1998 was coincident with one of the strongestE1 Nifio eventsof this century, and is considereda significantand unexpectedbenefit.  m and a standdensityof •830 stemsha-•  Introduction  respectively.  The temperature of the Northern Hemisphere has in-  The soil is  an Orthic Luvisol with a silty-clay texture and an 8-10 cm deep surfaceorganic layer. In 1994, the site contained about  9.9, 7.9 and3.6 kg C m-2 in the live biomass, detritusand mineralsoil layer, respectively[Goweret al., 1997; Chen et al., 1999]. Annual averageair temperatureand cumulative precipitationare about I øC and 400 mm [Chenet al., 1999], Half-hourly fluxes of CO2 (Fc, positive upward) were measuredusingthe eddy covariance(EC) techniqueat 39.5  creasedsignificantlyoverthe past 100 years [Nichollset al., m abovethe ground from February 2 to September 20, 1994 1996]. There is strong evidenceof an associatedincrease and from April 20, 1996 to December 31, 1998. The EC in biospheric activity because of increased growing season  sensors consisted  length [Keelinget al., 1996; Frolking,1997; Myneni et al.,  a closed-pathinfraredgasanalyzer[Chenet al., 1999]. Day-  1997; Menzel and Fabian, 1999; Randerson et al., 1999; Run-  of a 3-dimensional  sonic anemometer  and  time Fc was corrected by increasing its magnitude by the  ning et al., 1999a].However,the responseof the borealfor-  fraction(a functionof frictionvelocity,u.) requiredto close the forest energybalance (15-17 percent) [Blankenet al., 1998]. Nighttime F• was correctedby (i) applyingthe enin soil [Schlesinger et al., 1991],to climatewarming(espe- ergy balance closurecorrectionto high wind speed (u. > cially the responseof boreal soils) is not well understood 0.35m-•) fluxesand(ii) usingthe annualrelationships be[Sellerset al., 1997]. Previousstudieshave suggested that tweenthesecorrectednighttimefluxes(i.e. respiration(R))  est, which contains 13 percent of the carbon stored in the global terrestrial biomassand 43 percent of the C stored  early thaws due to warmer spring temperatures can result  in the net lossof C from borealblackspruce[Gouldenet al., 1998]and tundra [Oechelet al., 1993]ecosystems. Methods  and  Data  We investigatedthe responseof a boreal deciduousfor-  est (trembling aspen, PoputustremuloidesMichx. with scattered balsam poplar, Poputus ba!samiferaL. and hazel-  nut, CorytuscornutaMarsh. understory)to climate change by measuringnet ecosystemproductivity (NEP = -NEE, net ecosystemexchangeof CO2) for four years (1994 and 1996-98). This researchwas initiated as a part of the Boreal Ecosystem-Atmosphere Study (BOREAS) [Blacket at., 1996; Sellerset at., 1997]and has continuedunder the Boreal EcosystemResearchand Monitoring Sites (BERMS) programand the AmeriFlux Tower Network [Runnin9 et  at., 1999b].The studysite (53.7øN,106.2øW)is locatedin •Agroecology, Facultyof AgriculturalSciences,Universityof British Columbia, Vancouver, BC, Canada.  2now at EnvironmentalMonitoring Section, Canada Centre  and soil temperature at the 2-cm depth to replace low wind  speed(u. < 0.35 m s-•) fluxes[Blacket al., 1996]. The first correction, which increased high wind speed nighttime fluxesby 10-13 percentage,is consistentwith the results of a comparisonbetween EC fluxes and scaled-up chamber mea-  surementsin borealforests[Lavigneet al., 1997],while the second gave fluxes consistent with chamber measurements of soil CO• effiuxes at the site in low wind speed conditions  [Russellet al., 1998]. Flux measurements were not made in 1995, but climate and tree ring data indicated that 1995 fluxes were similar to 1997. NEP was calculated by sub-  tracting values of F• from the changesin CO• storage in  the air columnbelow the EC sensors[Yang et al., 1999]. Uncertainties in annual NEP values caused by measurement  uncertainty and gap filling were estimated to be ñ65, +60,  ñ35 and •50 g C m-• y-• in 1994,1996,1997,and 1998, respectively. Gross ecosystemphotosynthesis(GEP) was obtained by adding values of growing seasondaytime NEP to daytime R during the four years. R was calculated using the above mentioned annual ecosystemrespiration relationships and daytime soil temperatures at the 2-cm depth  [Blacket al., 1996]. Data gapsdue to measurementsched-  for Remote Sensing, Ottawa, ON, Canada.  3MeteorologicalServiceof Canada,Saskatoon,SK, Canada. 4Canadian Forest Service,Edmonton,AB, Canada. 5Meteorological Serviceof Canada,Downsview,ON, Canada.  ule, instrument malfunction and power failure were filled using linear interpolation and relationshipsbetween R and photosynthesisand various climatic and biologicalvariables.  Papernumber 1999GL011234.  Leaf area index (LAI) was measuredevery 2-3 weeksusing a LI-COR Inc. canopyanalyzer(modelLAI-2000) [Chen et al., 1997],exceptin 1996when it wasmeasuredoncein mid-  0094-8276/00/1999GL011234505.00  July. For the remainder of the 1996 growingseason,LAI was  Copyright2000 by the AmericanGeophysicalUnion.  1271  1272  BLACK ET AL.' WARM SPRINGS INCREASE CARBON SEQUESTRATION  BY A FOREST  Table 1. Productivity and Climate Statistics Description  Averageannualair temperature(øC) AverageApril-May air temperature(øC) Date of aspen leaf emergence Day of first detectable photosynthesis  Crowing season (CS)length(days) i Absorbed CS PAR(kmolphotons m-2)ii CS daytimeNEP (g C m-2) AnnualCEP (g C m-2) Annualecosystem respiration (g C m-2) AnnualNEP (g C m-2)  1994  1996  1.09  1997  -0.36 4.24  6.67  April 28 May 12  1998  2.74  3.13 9.89  5.93  May 19 May 31  May 8 May 19  April 10 May 1  134  128  134  154  2.04  1.89  2.12  2.54  727  619  692  834  1284  1181  1212  1420  1140  1101  1096  1130  144  80  116  290  iFromthe first to the last day of photosynthesis detectableby EC measurements. //Calculatedfor the CS asdescribed in [Chen et al., 1999]. The uncertaintiesare: date of leaf emergence-[-7days, first day of detectablephotosynthesis -[-3  days,CS length-[-6days,absorbed CS PAR(photosynthetically activeradiation)-[-0.05kmolphotons m-2, GSdaytime NEP -[-30g C m-2, annualCEP +100 g C m-2, annualecosystem respiration -Fl10g C m-2 andannualNEP -[-65,-[-60, -[-35and-t-50g C m-2 for the respective years.  calculated from incident PAR above and below the aspen  The impact of these differencesin photosynthetic activity  canopy[Chenet al., 1999]. Stemwoodand foliar C produc- is clearly evident in the cumulative NEP of the four years tion was estimated from tree ring widths measured at the (Figure lb and Table 1), with annual carbonsequestration 1.3-m height on 8 trees near the flux tower and annual leaf of 144-+-65, 80-+-60,116-+-35 and 290-t-50g C m-2 y-Z in fall (overstoryand understory)measuredusinglitter traps 1994, 1996, 1997 and 1998, respectively. Annual carbon se[Goweret al., 1997]. questration washighlycorrelated (r2 = 0.99)with spring Results The annual coursesof daily NEP are shown in Figure l a. During winter and early spring, values of NEP were neg-  air temperature. We attribute the large impact of spring air temperature on NEP to its associated impact on leaf emergence, and to the observation that annual maximum NEP  ative (i.e., respiratoryloss)and their magnitudeincreased with increasing air temperature. The sharp increase in NEP in spring indicated the occurrence of significant photosynthesis as a result of emerging and developing leaves. Car-  _(a)  AA•.•,•A  -  bonrelease intothe atmosphere wasmaximum in autumn  when theleaves had just senesced and soil temperatures  were highest fortheleafless forest. Themost striking differ-  _  ence inNEPbetween thefouryears wasinthetiming ofits increase inspring (Figure 1). Photosynthesis wasfirstde-  tectedinthedaytime ECfluxmeasurements onMay12,31,  .i  19 and 1 in 1994, 1996, 1997 and 1998, respectively(Table 1). This occurred12-21 days after the beginningof over-  I  storyaspenleafemergence (Figure2) and4-6 weeksafter snow melt. The first day of photosynthetic activity was detected from the decrease in daytime EC CO2 fluxes below  I  I  I  I  I  I  I  400  the trend in respiratoryfluxes. Daily (24-h) NEP began to increase2-3 days after this. The emergenceof the un-  2OO  derstory hazelnut leaves was slightly later than that of the overstory,but showedsimilar interannual differences.Aspen  ,/ //...  -,Y.,'.%1994  -  leafemergence datewashighlycorrelated (r2 - 0.99)with spring(April-May24-houraverage) air temperature (Figure3) andsignificantly correlated (r2 - 0.72)with spring soil temperature at the 2-cm depth. Air temperatures were well above normal during and immediately after the 199798 winter, and were likely the result of one of the strongest  -200  _'-'  -, d  E1Nifio SouthernOscillation(ENSO) eventsof this century occurringat this time [Mason et al., 1999]. The springair  , , , , ,F  M  A  M  d  ,J  A  S  O  N  D  Month  temperature in 1998 was 9.9 øC, which was 3.2, 5.7 and 4.0 øC higher than that in 1994, 1996 and 1997, respectively  Figure 1. (a) Daily net ecosystem productivity(NEP) (b) Cu-  (Table 1).  mulative  NEP.  BLACK ET AL.' WARM SPRINGS INCREASE CARBON SEQUESTRATION BY A FOREST occurs in the spring, when the days are relatively long and the temperatures are optimal for photosynthesis. These resuits have helped to quantify the effect of increasedgrowing seasonlength in this forest ecosystemand show that the seasonal-scaleclimate differenceswere more important than the differences in the annual means.  1273  20  r,.)  o  10  _  (a)  These results have also  shown that, because of the marked effect of inter-annual climatic variability on forest NEP, a few years of measurements of CO2 fluxes using the EC technique can provide an estimate of the sensitivity of the forest carbon balance to climatic change. Root-zone soil water content was generally high in 1994, 1996, 1997 and after June 15, 1998. Lack of rainfall between May 15 and June 15, 1998 causedsoil water content to drop significantly,which probably accountsfor the suddences-  "-  E  •  0  -10 ß  ._  -20  2  .--'/ -•//'" 1994 I  J  I  F  I  M  4  6  8 10 12  ".  Air Temr, t' øC "erature ) 1996 I  A  I  M  I  J  I  J  I  A  I  S  I  O  I  N  D  sation of leaf growth in late May (Figure 2). Despitethis drought in the growing season,annual carbon sequestration doubled in 1998, which was the year with the highest spring air temperature and earliest leaf emergencedate of the four years. 1998 illustrates two competing influencesof climate changeon NEP: spring warming, which promotes increased NEP, and drought stress,which reducesNEP. Differencesin annual NEP were largely due to differences  Month Figure 3, (a) Monthly averageair temperature measuredat 39.5 m abovethe ground (b) The relationshipbetweenApril-May average(24-hour) air temperatureand the day of the year when leaf emergence began.  in annualGEP. GEP in 1998wasover200 g C m-2 higher than in 1996, while ecosystemrespiration was about the  same(Table 1). One reasonthat annualGEP increasedwith earlier leaf emergenceis that the latter resulted in significantly higher total incident and absorbedphotosynthetically  duringthe growingseason(Table 1) becauseecosystem respiration was much less variable than photosynthesis in the four years. The variation of annual NEP over the four years was also apparent in stemwood and foliar carbon production. However, variation in the sum of these components of  active radiation (PAR) duringthe growingseason[Chenet al., 1999]. AbsorbedPAR totalsfor the growingseasonwere net primaryproductivity (NPP) (e.g.,259g C m-2 in 1996  2.04,1.89,2.12and2.54kmolphotonsm-2 for 1994,1996, rs. 285g C m-2 in 1998)wasmuchlessthan that in NEP  1997 and 1998, respectively, which closely correspondedto the pattern of annual GEP over the four years. Annual differencesin NEP were also similar to those in daytime NEP  suggesting the importanceof below-groundNPP (coarseand fine root growth)in this forest[Steeleet al., 1997].  Discussion I  I  I  I  I  and  Conclusions  I  This study has shown that, over the past five years, the highest carbon sequestrationby a boreal aspen ecosystem occurred during years with the warmest springs and earliest leaf emergence. Differences in spring temperature had  (a) Aspen  a larger impact oncarbon sequestration at thissitethan differences in annual mean temperature. Carbon sequestration doubled in 1998 during one of the strongest E1 Nifio x  SouthernOscillation(ENSO) eventsof this century,despite the coincident occurrence of drought during leaf develop-  ment. The increased NEP in 1998wasnot accompanied  3  (b)Hazelnut ,--.... / /  2  / 1998  -_ \ 1994 \  at a boreal black sprucesite [Gouldenet al., 1998]showing that earlier spring thaws can decreasecarbon sequestration as a result of increased soil respiration. The large increase in carbon sequestration by this ecosystem is considered a significant and unexpected benefit from spring weather at-  .'" .....'-:-•- \ :' ß .'  by increased respiration, as 1998 had cooler temperatures later in the year. These results are in contrast with findings  '  997  tributed  _.4•./.•i.-9•96I Apr May Jun  Jul  '.: Aug Sep Oct  Month Figure  2, Leaf area index (LAI) of the overstoryaspenand  understory hazelnut.  to the 1997-98  ENSO  event.  Acknowledgments. Funding was provided by NSERC (Collaborative Special Project and Operating Grants), MSCEnvironment Canada, CFS, Parks Canada, P ERD and NASA. We acknowledge the advice and assistance from many individuals: B. Goodison, J. Eley, R. Ketler, J. Chen, P. Blanken, P. Pacholek, U. Gramann, C. Hrynkiw, R. Swanson, G. Thurtell, R. Staebler, M. Novak, C. Russell, G. den Hartog, J. Deary, S. Chen, X. Lee, A. Wu, J. Olejnik, I. Simpson, and J. 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Sun and P.A. Arkin, The IRI seasonal climate prediction system and the 1997-1998 E1 Nifio Event, Bulletin of the American Meteorological Society, 80, 1853-1873, 1999. Menzel, A. and P. Fabian, Growing seasonextended in Europe, Nature 397, 659, 1999. Myneni, R.B., C.D. Keeling, C.J. Tucker, G. Asrar, R.R. Nemani, Increased plant growth in the northern high latitudes from 1981-1991, Nature, 386, 698-702, 1997. Nicholls, N., G.V. Gruza, J. Jouzel, T.R. Karl, L.A. Ogallo, D.E. Parker, Observed climate variability and change, in Climate Change 1995, edited by Houghton, J.T. et al., pp. 133-192, Cambridge University Press, Cambridge, 1996. Oechel, W.C., S.L. Hastings, G.L. Vourlitis, M.A. Jenkins, G. Riechers, N. Grulke, Recent change of arctic tundra ecosystems from a carbon sink to a source, Nature, 361, 520-523, 1993.  tion and flux in a boreal aspen forest, J. Geophys.Res., 106, 27653-27661, 1999.  T.A. Black, M.A. Arain, Z. Chen, Z. Nesic, P.C. Yang, Agroecology, Faculty of Agricultural Sciences, University of British Columbia, 266B, 2357 Main Mall, Vancouver,  BC, V6T 1Z4, Canada. (e-mail: ablack@interchange.ubc.ca; altafa@interchange.ubc.ca;zchen@unixg.ubc.ca;nesic@ppc.ubc. ca; chenggan@ unixg.ubc.ca) W.J. Chen, Environmental Monitoring Section, Canada Centre for Remote Sensing, 588 Booth Street, Ottawa, ON, KIA 0Y7,  Canada. (e-mail: wenjun'chen@geøcan'nrcan'gc'ca) A.G. Barr,  Meteorological Service of Canada, 11 Innova-  tion Boulevard, Saskatoon, SK, S7N 3H5, Canada. (e-mail: alan.barr@ec.gc.ca) E.H. Hogg, Canadian Forest Service, 5320-122 Street, Edmon-  ton, AB, T6H 3S5, Canada. (e-mail: thogg@nrcan.gc.ca) H.H. Neumann, Meteorological Service of Canada, 4905 Duf-  ferin Steet, Downsview, ON, M3H 5T4, Canada. (e-maih hneumann@ec.gc.ca)  (ReceivedNovember13, 1999;acceptedFebruary07, 2000.)  

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