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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 forest in years with a warm spring boreal deciduous T.A. Black, • W.J. Chen, •'2 A.G. Barr, a M.A. Arain, E.H. Hogg, 4H.H. Neumann s and P.C. Yang • • Z Nesic 1 • Z. Chen, . , Abstract. A boreal deciduous forest in Saskatchewan, Canada, sequestered 144i65, 80i60, 116-t-35 and 290-t-50 g C m -2 y-• in 1994, 1996, 1997 and 1998, respectively. The increased carbon sequestration was the result of a warmer spring and earlier leaf emergence, which significantly in- creased ecosystem photosynthesis, but had little effect on respiration. The high carbon sequestration in 1998 was co- incident with one of the strongest E1 Nifio events of this cen- tury, and is considered a significant and unexpected benefit. Introduction The temperature of the Northern Hemisphere has in- creased significantly over the past 100 years [Nicholls et al., 1996]. There is strong evidence of an associated increase in biospheric activity because of increased growing season length [Keeling et al., 1996; Frolking, 1997; Myneni et al., 1997; Menzel and Fabian, 1999; Randerson et al., 1999; Run- ning et al., 1999a]. However, the response of the boreal for- est, which contains 13 percent of the carbon stored in the global terrestrial biomass and 43 percent of the C stored in soil [Schlesinger t al., 1991], to climate warming (espe- cially the response of boreal soils) is not well understood [Sellers et al., 1997]. Previous studies have suggested that early thaws due to warmer spring temperatures can result in the net loss of C from boreal black spruce [Goulden et al., 1998] and tundra [Oechel et al., 1993] ecosystems. Methods and Data We investigated the response of a boreal deciduous for- est (trembling aspen, Poputus tremuloides Michx. with scattered balsam poplar, Poputus ba!samifera L. and hazel- nut, Corytus cornuta Marsh. understory) to climate change by measuring net ecosystem productivity (NEP = -NEE, net ecosystem exchange of CO2) for four years (1994 and 1996-98). This research was initiated as a part of the Bo- real Ecosystem-Atmosphere Study (BOREAS) [Black et at., 1996; Sellers et at., 1997] and has continued under the Bo- real Ecosystem Research and Monitoring Sites (BERMS) program and the AmeriFlux Tower Network [Runnin9 et at., 1999b]. The study site (53.7øN, 106.2øW) is located in •Agroecology, Faculty of Agricultural Sciences, University of British Columbia, Vancouver, BC, Canada. 2now at Environmental Monitoring Section, Canada Centre for Remote Sensing, Ottawa, ON, Canada. 3Meteorological Service of Canada, Saskatoon, SK, Canada. 4Canadian Forest Service, Edmonton, AB, Canada. 5Meteorological Service of Canada, Downsview, ON, Canada. Copyright 2000 by the American Geophysical Union. Paper number 1999GL011234. 0094-8276/00/1999GL011234505.00 Prince Albert National Park, Saskatchewan, Canada. This mature aspen forest was regenerated after a natural fire iv_ 1919 [Weir, 1996], and in 1998 had a mean height of 21.5 m and a stand density of •830 stems ha -• The soil is an Orthic Luvisol with a silty-clay texture and an 8-10 cm deep surface organic layer. In 1994, the site contained about 9.9, 7.9 and 3.6 kg C m -2 in the live biomass, detritus and mineral soil layer, respectively [Gower et al., 1997; Chen et al., 1999]. Annual average air temperature and cumulative precipitation are about I øC and 400 mm [Chen et al., 1999], respectively. Half-hourly fluxes of CO2 (Fc, positive upward) were measured using the eddy covariance (EC) technique at 39.5 m above the ground from February 2 to September 20, 1994 and from April 20, 1996 to December 31, 1998. The EC sensors consisted of a 3-dimensional sonic anemometer and a closed-path infrared gas analyzer [Chen et al., 1999]. Day- time Fc was corrected by increasing its magnitude by the fraction (a function of friction velocity, u.) required to close the forest energy balance (15-17 percent) [Blanken et al., 1998]. Nighttime F• was corrected by (i) applying the en- ergy balance closure correction to high wind speed (u. > 0.35 m -•) fluxes and (ii) using the annual relationships be- tween these corrected nighttime fluxes (i.e. respiration (R)) and soil temperature at the 2-cm depth to replace low wind speed (u. < 0.35 m s -•) fluxes [Black et al., 1996]. The first correction, which increased high wind speed nighttime fluxes by 10-13 percentage, is consistent with the results of a comparison between EC fluxes and scaled-up chamber mea- surements in boreal forests [Lavigne et al., 1997], while the second gave fluxes consistent with chamber measurements of soil CO• effiuxes at the site in low wind speed conditions [Russell et 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 changes in CO• storage in the air column below 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 ecosystem photosynthesis (GEP) was obtained by adding values of growing season daytime NEP to daytime R during the four years. R was calculated us- ing the above mentioned annual ecosystem respiration rela- tionships and daytime soil temperatures at the 2-cm depth [Black et al., 1996]. Data gaps due to measurement sched- ule, instrument malfunction and power failure were filled using linear interpolation and relationships between R and photosynthesis and various climatic and biological variables. Leaf area index (LAI) was measured every 2-3 weeks using a LI-COR Inc. canopy analyzer (model LAI-2000) [Chen et al., 1997], except in 1996 when it was measured once in mid- July. For the remainder of the 1996 growing season, LAI was 1271 1272 BLACK ET AL.' WARM SPRINGS INCREASE CARBON SEQUESTRATION BY A FOREST Table 1. Productivity and Climate Statistics Description 1994 1996 1997 1998 Average annual air temperature (øC) Average April-May air temperature (øC) Date of aspen leaf emergence Day of first detectable photosynthesis Crowing season (CS) length (days) i Absorbed CS PAR (kmol photons m-2) ii CS daytime NEP (g C m -2) Annual CEP (g C m -2) Annual ecosystem respiration (g C m -2) Annual NEP (g C m-2) 1.09 -0.36 2.74 3.13 6.67 4.24 5.93 9.89 April 28 May 19 May 8 April 10 May 12 May 31 May 19 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 iFrom the first to the last day of photosynthesis detectable by EC measurements. //Calculated for the CS as described in [Chen et al., 1999]. The uncertainties are: date of leaf emergence -[-7 days, first day of detectable photosynthesis -[-3 days, CS length -[-6 days, absorbed CS PAR (photosynthetically ctive radiation) -[-0.05 kmol photons m -2, GS daytime NEP -[-30 g C m -2, annual CEP +100 g C m -2, annual ecosystem respiration -Fl10 g C m -2 and annual NEP -[-65, -[-60, -[-35 and -t-50 g C m -2 for the respective years. calculated from incident PAR above and below the aspen canopy [Chen et al., 1999]. Stemwood and foliar C produc- tion was estimated from tree ring widths measured at the 1.3-m height on 8 trees near the flux tower and annual leaf fall (overstory and understory) measured using litter traps [Gower et al., 1997]. Results The annual courses of daily NEP are shown in Figure l a. During winter and early spring, values of NEP were neg- ative (i.e., respiratory loss) and their magnitude increased with increasing air temperature. The sharp increase in NEP in spring indicated the occurrence of significant photosyn- thesis as a result of emerging and developing leaves. Car- bon release into the atmosphere was maximum in autumn when the leaves had just senesced and soil temperatures were highest forhe leafless forest. The most riking differ- ence in NEP between the four years was in the timing of its increase in spring (Figure 1). Photosynthesis wa  f rst de- tected in the daytime EC flux measurements on May 12, 31 , 19 and 1 in 1994, 1996, 1997 and 1998, respectively (Table 1). This occurred 12-21 days after the beginning of over- story aspen leaf emergence (Figure 2) and 4-6 weeks after snow melt. The first day of photosynthetic activity was de- tected from the decrease in daytime EC CO2 fluxes below the trend in respiratory fluxes. Daily (24-h) NEP began to increase 2-3 days after this. The emergence of the un- derstory hazelnut leaves was slightly later than that of the overstory, but showed similar interannual differences. Aspen leaf emergence date was highly correlated (r2 - 0.99) with spring (April-May 24-hour average) air temperature (Fig- ure 3) and significantly correlated (r 2 - 0.72) with spring soil temperature at the 2-cm depth. Air temperatures were well above normal during and immediately after the 1997- 98 winter, and were likely the result of one of the strongest E1 Nifio Southern Oscillation (ENSO) events of this century occurring at this time [Mason et al., 1999]. The spring air 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 (Table 1). The impact of these differences in photosynthetic activity is clearly evident in the cumulative NEP of the four years (Figure lb and Table 1), with annual carbon sequestration of 144-+-65, 80-+-60, 116-+-35 and 290-t-50 g C m -2 y-Z in 1994, 1996, 1997 and 1998, respectively. Annual carbon se- questration was highly correlated (r 2 = 0.99) with spring air temperature. We attribute the large impact of spring air temperature on NEP to its associated impact on leaf emer- gence, and to the observation that annual maximum NEP 400 2OO -200 _ (a) AA•.•,•A - _ .i I I I I I I I I ,/ //... -,Y.,'.% 1994 - _'-' - , , , , , , - d F M A M d ,J A S O N D Month Figure 1. (a) Daily net ecosystem productivity (NEP) (b) Cu- mulative NEP. BLACK ET AL.' WARM SPRINGS INCREASE CARBON SEQUESTRATION BY A FOREST 1273 occurs in the spring, when the days are relatively long and the temperatures are optimal for photosynthesis. These re- suits have helped to quantify the effect of increased growing season length in this forest ecosystem and show that the seasonal-scale climate differences were more important than the differences in the annual means. These results have also shown that, because of the marked effect of inter-annual climatic variability on forest NEP, a few years of measure- ments 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 caused soil water content to drop significantly, which probably accounts for the sudden ces- sation of leaf growth in late May (Figure 2). Despite this drought in the growing season, annual carbon sequestration doubled in 1998, which was the year with the highest spring air temperature and earliest leaf emergence date of the four years. 1998 illustrates two competing influences of climate change on NEP: spring warming, which promotes increased NEP, and drought stress, which reduces NEP. Differences in annual NEP were largely due to differences in annual GEP. GEP in 1998 was over 200 g C m -2 higher than in 1996, while ecosystem respiration was about the same (Table 1). One reason that annual GEP increased with earlier leaf emergence is that the latter resulted in signifi- cantly higher total incident and absorbed photosynthetically active radiation (PAR) during the growing season [Chen et al., 1999]. Absorbed PAR totals for the growing season were 2.04, 1.89, 2.12 and 2.54 kmol photons m -2 for 1994, 1996, 1997 and 1998, respectively, which closely corresponded to the pattern of annual GEP over the four years. Annual dif- ferences in NEP were also similar to those in daytime NEP 20 r,.) o 10 "- 0 E • -10 ._ -20 _ (a) ß 2 4 6 8 10 12 ". //'" .--'/ Air Temr, e ature t øC 1996 -• 1994 " ' ) - I I I I I I I I I I I J F M A M J J A S O N D Month Figure 3, (a) Monthly average air temperature measured at 39.5 m above the ground (b) The relationship between April-May average (24-hour) air temperature and the day of the year when leaf emergence began. during the growing season (Table 1) because cosystem res- piration 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 produc- tion. However, variation in the sum of these components of net primary productivity (NPP) (e.g., 259 g C m -2 in 1996 rs. 285 g C m -2 in 1998) was much less than that in NEP suggesting the importance of below-ground NPP (coarse and fine root growth) in this forest [Steele et al., 1997]. x I I (a) Aspen I I I I (b) Hazelnut ,-- .... -_ 3 / \ 1994 / \ 2 / .'" ..... '-:-•- \ 1998 :' ' ß .' 997 _.4•./.•i.- 9•96 I '.: Apr May Jun Jul Aug Sep Oct Month Figure 2, Leaf area index (LAI) of the overstory aspen and understory hazelnut. Discussion and Conclusions This study has shown that, over the past five years, the highest carbon sequestration by a boreal aspen ecosystem occurred during years with the warmest springs and earli- est leaf emergence. Differences in spring temperature had a larger impact on carbon sequestration at this site than differences in annual mean temperature. Carbon sequestra- tion doubled in 1998 during one of the strongest E1 Nifio Southern Oscillation (ENSO) events of this century, despite the coincident occurrence of drought during leaf develop- ment. The increased NEP in 1998 was not accompanied by increased respiration, as 1998 had cooler temperatures later in the year. These results are in contrast with findings at a boreal black spruce site [Goulden et al., 1998] showing that earlier spring thaws can decrease carbon 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- tributed to the 1997-98 ENSO event. Acknowledgments. Funding was provided by NSERC (Collaborative Special Project and Operating Grants), MSC- Environment Canada, CFS, Parks Canada, P ERD and NASA. We acknowledge the advice and assistance from many individ- uals: 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. Fuentes. 1274 BLACK ET AL.- WARM SPRINGS INCREASE CARBON SEQUESTRATION BY A FOREST References Black, T.A., G. den Hartog, H.H. Neumann, P.D. Blanken, P.C. Yang, C. Russell, Z. Nesic, X. Lee, S.G. Chen, R. Staebler, and M.D. Novak, Annual cycles of water vapour and carbon diox- ide fluxes in and above a boreal aspen forest, Global Change Biology, 2, 101-111, 1996. Blanken, P.D., T.A. Black, H.H. Neumann, G. den Hartog, P.C. Yang, Z. Nesic, R. Staebler, W. Chen and M.D. Novak, Tur- bulent flux measurements above and below the overstory of a boreal aspen forest, Boundary-Layer Meteorology, 89, 109-140, 1998. Chen, J.M., P.D. Blanken, T.A. Black, M. Guilbeault, S.G. Chen, Radiation regime and canopy architecture in a boreal aspen forest, Agricultural and Forest Meteorology, 86, 107-125, 1997. Chen, W. J., T.A. Black, P.C. Yang, A.G. Barr, H.H. Neffmann, Z. Nesic, P.D. Blanken, M.D. Novak, J. Eley, R.J. Ketler and R. Cuencas, Effects of climate variability on the annual carbon sequestration by a boreal aspen forest, Global Change Biology, 5, 41-53, 1999. Frolking, S. J., Sensitivity of spruce/moss boreal forest net ecosys- tem productivity to seasonal anomalies in weather, J. Geophys. Res., 102, 29053-29064, 1997. Goulden, M.L., S.C. Wofsy, J.W. Harden, S.E. Trumbore, P.M. Grill, S.T. Gower, T. Fries, B.C. Daube, S.M. Fan, D.J. Sutton, A. Bazzaz and J.W. Munger, Sensitivity of boreal forest carbon balance to soil thaw, Science, 279, 214-217, 1998. Gower, S.T., J.G Vogel, J.M. Norman, C.J. Kucharik, S.J. Steele and T.K. Stow, Carbon distribution and above ground net primary production in aspen, jack pine and black spruce stands in Saskatchewan and Manitoba, Canada, J. Geophys. Res., 102, 29029-29041, 1997. Keeling, C.D., J.F.S. Chin, T.P. Whorl, Increased activity of northern vegetation inferred from atmospheric CO2 observa- tions, Nature, 382, 146-149, 1996. Lavigne, M., M.G. Ryan, D.E. Anderson, D.D. Baldocchi, P.M. Grill, D.R. Fitzjarrald, M.L. Goulden, S.T. Gower, J.M. Massheder, J.H.McCaughey, M. Rayment and R.G. Striegl, Comparing nocturnal eddy covariance measurements to esti- mates of ecosystem respiration made by scaling chamber mea- surements at six coniferous boreal sites, J. Geophys. Res., 102, 28977-28985, 1997. Mason, S.J., L. Goddard, N.E. Graham, E. Yulaeva, L. Sun and P.A. Arkin, The IRI seasonal climate prediction system and the 1997-1998 E1 Nifio Event, Bulletin of the American Mete- orological Society, 80, 1853-1873, 1999. Menzel, A. and P. Fabian, Growing season extended 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. 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Hibbard, A global terrestrial monitoring net- work: integrated tower fluxes, flask sampling, ecosystem mod- elling and EOS satellite data, Remote Sensing. Environment, In press, 1999b. Russell C.A., R.P. Voroney, T.A. Black, P.D. Blanken, P.C. Yang, Carbon dioxide effl. ux from the floor of a boreal aspen forest. Evaluation of methods-verfication by infra-red analysis of a dynamic closed chamber, Canadian Journal of Soil Science, 87, 311-316, 1998. Schlesinger, W. H., Biogeochemistry: An Analysis of Global Change, Academic, San Diego, California, 1991. Sellers, P. J., et al., BOREAS in 1997: Experiment overview, scientific results, and future directions, J. Geophys. Res., 102, 28731-28769, 1997. Steele, S.J.S.T. Gowerl J.G. Vogel, J.M. Norman, Root mass, net primary production and turnover in aspen, jack pine and black spruce forests in Saskatchewan and Manitoba, Canada, Tree Physiology, 17, 577-587, 1997. Weir, J., The fire frequency and age mosaic of a mixedwood boreal forest, M.Sc. thesis, University of Calgary, Canada, 1996. Yang, P. C., T.A. Black, H.H. Neumann, M.D. Novak and P.D. Blanken, Spatial and temporal variability of CO2 concentra- 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, Univer- sity 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) (Received November 13, 1999; accepted February 07, 2000.)

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