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N2O emissions and carbon sequestration in a nitrogen-fertilized Douglas fir stand Jassal, Rachhpal S.; Black, T. Andrew; Chen, Baozhang; Roy, Real; Nesic, Zoran; Spittlehouse, D. L.; Trofymow, J. A. 2008

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N2O emissions and carbon sequestration in a nitrogen-fertilizedDouglas fir standRachhpal S. Jassal,1T. Andrew Black,1Baozhang Chen,1Real Roy,2Zoran Nesic,1D. L. Spittlehouse,3and J. A. Trofymow4Received 23 April 2008; revised 23 July 2008; accepted 18 August 2008; published 4 November 2008.[1] This study investigated how nitrogen (N) fertilization with 200 kg N haC01of a 58-year-old West Coast Douglas fir stand influenced its net greenhouse gas (GHG) global warmingpotential (GWP) in the first year after fertilization. Effects of fertilization on GHG GWPwere calculated considering changes in soil N2O emissions, measured using the staticchamber technique and the soil N2O gradient technique; eddy covariance (EC) measurednet ecosystem productivity (NEP); and energy requirements of fertilizer production,transport, and its aerial spreading. We found significant N2O losses in fertilized plotscompared to a small uptake in nonfertilized plots. Chamber-measured N loss in thefertilized plots was about 16 kg N2OhaC01in the first year, which is equivalent to 10 kg NhaC01or 5% of the applied fertilizer N. Soil N2O emissions measured using the gradienttechnique, however, exceeded the chamber measurements by about 50%. We alsocompared a polymer-coated slow-release urea with regular urea and found that the formerdelayed N2O emissions but the year-end total loss was about the same as that from regularurea. Change in NEP due to fertilization was determined by relating annual NEP for thenonfertilized stand to environmental controls using an empirical and a process-basedmodel. Annual NEP increased by 64%, from 326 g C mC02, calculated assuming that thestand was not fertilized, to the measured value of 535 g C mC02with fertilization. At the endoftheyear,netchangeinGHGGWPwasC02.28tCO2haC01comparedtowhatitwouldhavebeen without fertilization, thereby indicating favorable effect offertilization even in the firstyear after fertilization with significant emissions of N2O.Citation: Jassal, R. S., T. A. Black, B. Chen, R. Roy, Z. Nesic, D. L. Spittlehouse, and J. A. Trofymow (2008), N2O emissions andcarbon sequestration in a nitrogen-fertilized Douglas fir stand, J. Geophys. Res., 113, G04013, doi:10.1029/2008JG000764.1. Introduction[2] Forests play a key role in the natural carbon (C) cycle.Each year forests absorb billions of tons of CO2, a highproportion of which is lost when trees respire and also in thedecomposition of soil organic matter and forest floor litter.In an east-west transect study of Canadian forests andpeatlands, intermediate-aged stands (35–60 years old)showed the highest maximum net ecosystem productivity(NEP) and gross primary productivity (GPP) [Coursolle etal., 2006]. Our recent research shows that a 58-year-oldWest Coast Douglas fir sequesters 2–3 t C haC01yC01[Humphreys et al., 2006; Jassal et al., 2007]. Weather canhave a significant impact on C exchange. It was found thatwarmer temperatures associated with El Nin˜o caused anincrease in C emissions, reducing the net amount of Csequestered [Morgenstern et al., 2004]. In the coastalregions of British Columbia, which have very little nitrogen(N) deposition from pollution sources owing to their remotelocation, and soils deficient in N [Hanley et al., 1996],Douglas fir stands respond to N fertilization [Brix, 1991;Fisher and Binkley, 2000; Chapin et al., 2002]. Thestandard forest fertilization application rate in West Coastforests is 200 kg N haC01from prilled urea [Hanley et al.,1996]. While fertilization of stands of midrotation trees (i.e.,of commercial thinning size, 20–40 years old) can result inadditional merchantable timber volumes, fertilization late inthe rotation may be the most attractive alternative econom-ically. A single application 8–10 years before the finalharvest of near-end-of-rotation (50–60-year-old) Douglasfir stands provides an attractive financial return with avolume growth increase of about 20% on average sites[Hanley et al., 1996]. Also, fertilization is one of the eligiblemanagement practices for C sequestering and hence reduc-ing CO2emissions under Article 3.4 of the Kyoto Protocol.[3] Simulated chronic N deposition has been shown toincrease C storage in northern temperate forests [Pregitzeret al., 2008]. In a meta-analysis, Johnson and Curtis [2001]JOURNAL OF GEOPHYSICAL RESEARCH, VOL. 113, G04013, doi:10.1029/2008JG000764, 20081Biometeorology and Soil Physics Group, University of BritishColumbia, Vancouver, British Columbia, Canada.2Department of Biology, University of Victoria, Victoria, BritishColumbia, Canada.3Research Branch, Ministry of Forests and Range, Victoria, BritishColumbia, Canada.4Canadian Forest Service, Natural Resources Canada, Victoria, BritishColumbia, Canada.Copyright 2008 by the American Geophysical Union.0148-0227/08/2008JG000764$09.00G04013 1of10found that N fertilization was the only forest managementpractice that had a clearly positive effect on the soil C pool.Steadily rising atmospheric CO2may likely stimulate theeffect of N deposition and fertilization resulting in increasedforest biomass [Nadelhoffer et al., 1999]. Leggett andKelting [2006] found that N fertilization of loblolly pineplantations not only increased aboveground and below-ground biomass but also significantly increased soil C.The increase in soil C storage with N fertilization has beenattributed, in part, to an increase in litter inputs as a result ofhigher plant production and partly to reduced decomposi-tion rates of soil organic matter and humus [Magill andAber, 1998; Prescott, 1995]. Olsson et al. [2005] found thatfertilization of a boreal Norway spruce stand led to athreefold increase in aboveground productivity, possiblybecause of decreased C allocation to roots in response tohigher nutrient availability.[4] Another major concern with N fertilization is thepotential loss of applied fertilizer N, e.g., NH3volatiliza-tion, nitrate leaching, and denitrification, resulting in pos-sible negative environmental impacts. Losses of N inammonia volatilization, when fertilizer is applied to well-drained and acidic forest soils (pH C24 5) under wet and coolconditions, are likely to be small [Rachhpal-Singh and Nye,1986]. Chappell et al. [1999] found that net nitrificationrates following repeated (8–10 years) N fertilization ofcoastal Douglas fir stands were higher than those in theunfertilized stands. N losses in denitrification have beenextensively studied in agricultural crops [e.g., Pattey et al.,2007] and in grazed pastures [e.g., Liebig et al., 2006], butfew studies have been conducted on denitrification losses inforest soils following fertilizer N application. Pang and Cho[1984] reported negligible denitrification loss of N whenforest soils from Shawnigan Lake, British Columbia, wereincubated with different rates of fertilizer N. Schiller andHastie [1996], using static chambers, measured N2O lossesfrom lowland, drained lowland, clear-cut, and upland borealforests near Cochrane, Ontario, and found an emission of3.1 mgN2OmC02hC01from an unvegetated clear-cut sitecompared to an uptake of 7.7 mgN2OmC02hC01at a drainedlowland site. Liebig et al. [2006] reported that fertilizedcrested wheatgrass enhanced deep storage of soil organic Cbut resulted in greater N2O emissions relative to nativenonfertilized pastures in the northern Great Plains. However,little is known about denitrification losses in N-fertilizedforest soils. The current Intergovernmental Panel on ClimateChange (IPCC) guidelines assume that 1.25% of fertilizer Nis lost as N2O and NO. These estimates, taken fromNational Greenhouse Gas Inventory Committee (NGGIC)[2001], are based on fertilizer application in farming sys-tems. In coniferous forest soils, highly mobile NO3C0may getconverted into less mobile N because of microbial assimi-lation of NO3C0followed by a release of biomass N as organicN and NH4+[Stark and Hart, 1997], thereby minimizingNO3C0leaching and denitrification losses of N.[5] While it is necessary to determine and quantify theeffects of N fertilization on stand C sequestration (i.e.,NEP), it is also important to address environmental con-cerns by measuring N2O emissions to determine the netgreenhouse gas (GHG) global warming potential (GWP).The GWP of N2O is 296 times (100-year time horizon)greater than that of CO2[Ehhalt and Prather, 2001], yetthere is little information on its net radiative forcing as aresult of forest fertilization.[6] We report the effects of N fertilization of a 58-year-old West Coast Douglas fir stand with 200 kg N haC01onsoil N2O emissions and stand NEP. We also calculate the netchange in GHG GWP resulting from forest fertilization byaccounting for N2O emissions and energy costs of fertilizerproduction, transport, and application. We also comparepolymer-coated slow-release urea (Environmentally SmartNitrogen (ESN), Agrium Inc., Calgary, Alberta, Canada) toregular urea for its potential effectiveness in reducing N2Oemissions from the forest floor.2. Materials and Methods2.1. Site Description[7] Measurements were made in a 58-year-old Douglasfir stand (C24130 ha) located about 10 km southwest ofCampbell River (49C1765207.800N, 125C1762006.300W, flux towerlocation), on the east coast of Vancouver Island, Canada.The soil is a humo-ferric podzol (Quimper sandy loam) witha variable surface litter-fermenting-humified organic layer0–6 cm thick and underlain with a dense compacted till at adepth of 1 m [Jungen, 1986]. Below the organic layer, soiltexture gradually changes to gravelly loamy sand in theupper 40 cm and to gravelly sand with increasing depth.The mean annual temperature and precipitation at the siteare 8.6C176C and 1450 mm, respectively, and the site isoccasionally subjected to a soil water deficit in August,September, and October. Further details on soil and vegeta-tion characteristics can be found in the work by Humphreyset al. [2006].2.2. Climate and Eddy Covariance Measurements[8] Climate and eddy covariance (EC) instrumentationand measurements at this site are described in detail byJassal et al. [2007], Humphreys et al. [2006], andMorgenstern et al. [2004]. Briefly, EC fluxes were mea-sured at the 43-m height using a three-axis sonic anemom-eter (model R3, Gill Instruments Ltd., Lymington, UK) andan infrared gas analyzer (IRGA) (model LI-6262, LI-CORInc., Lincoln, Nebraska, USA) in a temperature-controlledhousing with a heated 4-m-long air sampling tube. CO2concentrations were measured at four heights using amanifold, pump, and LI-840 IRGA to estimate half-hourlychanges in CO2storage in the air column beneath the ECsensors. Half-hourly measurements of soil water contentand soil temperature profiles were made continuously nearthe EC flux tower. At two locations, soil volumetric watercontent (q) was measured at 1–2-, 10–12-, 35–48-, and70–100-cm depths using 30-cm-long water content reflec-tometers (model CS-615, Campbell Scientific Inc., Logan,Utah, USA). Soil temperature (Ts) measurements were madeat the 5-, 10-, 20-, 50-, and 100-cm depths with copper-constantan thermocouples. Downwelling photosyntheticallyactive radiation (Q) was measured at the canopy height witha quantum sensor (model LI-190SB, LI-COR Inc.). Airtemperature (Ta) and relative humidity were measured atthe height of the EC instrumentation (43 m above the groundsurface) using a temperature and humidity probe (modelHMP-35C, Vaisala Oyj, Helsinki, Finland). Precipitation(P) was measured using two tipping-bucket rain gaugesG04013 JASSAL ET AL.: GHG BUDGET OF AN N-FERTILIZED FOREST2of10G04013(model 2501, Sierra Misco, Berkeley, California, USA)mounted on the flux tower at the 25-m height and a precip-itation gauge (model I-200B, Geonor A. S., Oslo, Norway)(for determining the water equivalent of snowfall in winter)installed in a young Douglas fir plantation about 3 km fromthe site.[9] Net ecosystem exchange (NEE) was calculated as thesum of the half-hourly EC-measured flux of CO2(FC) andthe rate of change in CO2storage (FS) in the air columnbetween the ground and the EC measurement level. FCwascalculated using FC= raw0s0c, where rais the mean molardensity of dry air at sensor height and w0s0cis the covariancebetween the vertical wind velocity (w) and the mole mixingratio of CO2(sc), after making a three-axis coordinaterotation so that the mean vertical and lateral componentsof wind velocity and the covariance between them wereequal to zero [Humphreys et al., 2006]. The overbar andprime denote time average (half hour) and fluctuation fromthe average, respectively. FSwas approximated by FS=hmraDsc/Dt [Hollinger et al., 1994; Morgenstern et al.,2004], where hmis the EC measurement height (i.e., 43 m),Dscis the difference between the average (half-hourlymean) CO2mixing ratio measured at the EC level (sc)ofthe following and previous half hours, and Dt = 3600 s.NEP, which is the net C sequestered by the ecosystem, wascalculated as NEP = C0NEE.2.3. Stand Fertilization[10] On the West Coast, fertilizer is usually appliedaerially to forest stands during late fall, winter, or earlyspring with cool, wet, and windless weather in fog-freeconditions. Under these weather and nongrowing condi-tions, (1) losses of applied N through ammonia volatiliza-tion are minimal, (2) intercepted fertilizer does not stay longon the foliage and gets washed to the ground, and (3) directfoliar uptake of N is small. An area of 1115 ha of Douglasfir forest on TimberWest Forest Corp. land on the east coastof Vancouver Island was aerially fertilized with urea at 200kg N haC01during 11–15 January 2007 using a EurocopterSA315B helicopter (Western Aerial Applications Ltd.,Chilliwack, British Columbia, Canada) with an in-house-engineered hydraulic-driven spreader bucket and a GPS-assisted guidance system. A block of 390-ha forest fertilizedon 13 January included the DF49 EC flux tower footprintarea. A nonfertilized area of about 17 ha (200 m C2 850 m)on the southeast side of the fertilized block (500 m from theflux tower) served as a control for comparing differences intree growth, C stocks, and greenhouse gas emissions.Location of the control area was chosen to minimize thenumber of times the tower footprint included winds blowingover the control area (winds from this direction accountedfor only 5% of wind directions during the year). Weobserved that on the day of fertilizer application, about halfof the fertilizer was retained in the snow-laden foliage,which was washed to the ground surface with the melting ofintercepted snow in the following days.2.4. Measurement of Soil N2O Effluxes[11] To study the effect of fertilization on soil N2Oemissions, and to compare regular urea to slow-release urea(ESN), we established a randomized complete block design(RCBD) experiment with a control and the two types ofurea, with four replications, on twelve 100-m2plots in theunfertilized (control) area. Fertilizer treatment at 200 kg NhaC01with urea and ESN of these plots was done manuallyon 11 April 2007, and N2O efflux measurements began on12 April and continued every 2–3 weeks until the end of theyear.[12] To determine soil N2O efflux, we used the staticchamber technique following the procedure described bySchiller and Hastie [1996]. PVC cylindrical collars of 21-cmdiameter and 10-cm length were installed and firmly securedup to 5 cm deep in the soil. Before each measurement,Plexiglas circular covers, each with a vent tube and siliconrubber septum (Soil Moisture Systems, Tucson, Arizona,USA) at the top, fitted with a small fan underneath (with a9-V battery secured at the top), were placed on the collars.Each cover had two circular rubber seals that allowed thecover to fit firmly to the collar, thus avoiding leaks, whilethe fan, directed upward, ensured proper mixing of thechamber headspace during efflux measurement. Gas sam-ples of 20 cm3from the chamber headspace were drawnwith a syringe from near the soil surface immediately beforeplacing the cover and at 3, 10, 20, and 30 min after placingthe cover and were transferred to preevacuated 12-cm3vials(Exetainers, Labco Limited, Buckinghamshire, UK). Thesesamples were analyzed in the laboratory on a gas chromato-graph (model 3800, Varian Inc., Palo Alto, California, USA)fitted with an electron capture detector using 5% methanebalance argon as the carrier gas within 24 h of sampling.The N2O mixing ratio (sN2O) of the samples was determinedby comparing with zero and 1-ppbv standards, which wererun twice, once before and once after the samples. Theagreement between replicate samples at ambient concen-trations was very good, differing by less than 1%. TheExetainers tested by storing gas samples of varying con-centrations up to 6 weeks maintained a vacuum quite well.While fresh supplies of Exetainers shipped by air directlyfrom the manufacturers in the United Kingdom were ex-ceptionally well sealed, about 8% of the vials from theprevious year had lost vacuum. However, we discarded anyvials not showing enough suction at the time of injection ofsamples in the field.[13] The increase in chamber headspace sN2Oover thesampling time (up to 30 min) was generally nonlinear,especially when emissions were high, so the rates of changein sN2O(dsN2O/dt, mmol molC01hC01) were obtained fromeither a linear increase up to 10 min or a logarithmic fit upto 30 min. The N2O efflux (FN2O, mmol mC02hC01) wascalculated using FN2O=(raV/A)dsN2O/dt, where rais themolar density (mol mC03)ofdryair,V is the volume (m3)ofthe chamber headspace, and A is the cross-sectional area(m2) of the collar.[14] We also compared the chamber N2O effluxes withthose obtained using the soil N2O gradient technique. On11 July 2007, we inserted pointed 2-mm outer-diameter,35-cm-long stainless steel gas-sampling tubes, each fittedwith a silicone rubber septum at the top, into the groundnear each collar. The tubes were bent at C2460C176 and pushed atthis angle from the vertical so that the 10-cm-long perfo-rated end of each tube was positioned horizontally 5 cmbelow the surface. Immediately after insertion, we pumpedair into each tube to remove any soil particles blocking theperforations that could have occurred when the tubes wereG04013 JASSAL ET AL.: GHG BUDGET OF AN N-FERTILIZED FOREST3of10G04013pushed into the ground. Gas samples from the 5-cm depthand the soil surface were also taken and injected into theExetainers, generally in duplicate, before and after thechamber samplings and analyzed as above. Soil N2Oeffluxes were calculated using Fick’s first law as FN2O=DsdCN2O/dz, where Ds, the diffusivity of the N2Ointhesurface soil layer (m2hC01), was obtained from measuredsoil water content and bulk density values and dCN2O/dz isthe N2O concentration gradient between 5-cm depth and thesoil surface (mmol mC04), with CN2Ocalculated from rasN2O.We used the relationship Ds= 1.18Dme2.28obtained fromdiffusivity measurements on soil cores taken from this sitebut at a location about 200 m away from these measure-ments [Jassal et al., 2005], where Dmis the moleculardiffusivity of N2O (0.051 m2hC01at 20C176C) and e is thefractional air-filled porosity.2.5. Calculation of Net GHG GWP[15] We calculated the net GHG budget in the first yearafter fertilization by considering the CO2equivalence of thenet change in soil N2O emissions, the net change in NEPafter adjusting for climate variability, and the GHG equiv-alence of energy needed for the manufacturing, transport,and aerial application of fertilizer urea. The CO2equivalentof soil N2O emissions was calculated by multiplying the netN2O loss by 296 [Ehhalt and Prather, 2001]. The netchange in NEP due to fertilization was computed using anempirical model and a process-based model. The formerwas developed by relating (using multiple-linear regression)the annual NEP values prior to fertilization to climaticfactors. The latter was the EASS-BEPS, a land surfaceand ecosystem model, [Chen et al., 2007a, 2007b] coupledwith the PnET-CN C balance model [Aber et al., 1997] andwas run at half-hourly time steps for 1998–2007. Keyparameters were estimated using an inverse algorithm withmeasured meteorological and EC data for 2001–2006.Since any change in soil CO2efflux is included in themeasurement of NEP, there was no need to account this forthe purpose of the calculation of net change in GHG GWPfollowing fertilization.[16] The Eurocopter SA315B consumed 8 L of JetA fuelper hectare, which is equivalent to 20 kg CO2haC01usingthe conversion in the IPCC guidelines for national green-house gas inventories. The CO2equivalent of the fertilizerwas calculated from the energy requirement of fertilizerproduction and its transport at 40 MJ kgC01N[Kongshaug,1998; Ozkan et al., 2004]. Any change in soil CO2effluxdue to fertilization, including that released upon ureahydrolysis ((NH2)2CO + 3H2O ! 2NH4++ 2OHC0+CO2)and reduction of N2OtoN2(i.e., 2N2O+CH2! CO2+H2O+2N2), in the surface labile-C-rich layer is accountedfor in the measurement of NEP. The energy equivalent ofhuman labor, calculated as the CO2equivalent of 4 manhours per hectare of forest fertilization at 2 MJ hC01[Ozkanet al., 2004], was negligible compared to fossil fuel energyinvolved in the manufacturing, transport, and application offertilizer.[17] While the focus of this study was to report change incalculated GHG GWP, arising because of changes in soilN2O emissions and NEP, at DF49, we also report results onthe effect of fertilization on NEP at two other nearbyDouglas fir stands, a 19-year-old stand (HDF88) and a7-year-old plantation (HDF00) (for site details, seeHumphreys et al. [2006]). While the 58- and 19-year-oldstands were similarly fertilized,the 7-year-oldstand, becauseof its young age and competing understory, was fertilizedmanually at 80-g urea per tree along the tree’s drip line.3. Results3.1. Weather[18] The weather variables Ta, q, P, and Q followed thesame general seasonal trend between years (Figure 1).While the 5-day mean Taduring 2007 varied about the9-year mean, P was well distributed, so that summertime(July–September) q was the highest in the 10-year siterecord, indicating the absence of the generally observedsummer drought, which limits productivity at this site[Jassal et al., 2007]. However, because of cloudy weather,annual Q was about 7% lower than the 9-year mean,suggesting possible growth limitation during 2007 due tolow Q [Morgenstern et al., 2004].3.2. C Exchange Between the Atmosphere and theForest Ecosystem[19] Figure 2 shows that fertilization increased annualNEP at all three sites in this West Coast Douglas firchronosequence. It also suggests that a near-end-of-rotationFigure 1. Interannual variations in 5-day mean airtemperature (Ta), 0–30-cm soil water content (q), cumula-tive precipitation (P), and cumulative total photosyntheti-cally active radiation (Q) at the 58-year-old West CoastDouglas fir stand.G04013 JASSAL ET AL.: GHG BUDGET OF AN N-FERTILIZED FOREST4of10G04013stand, DF49, has reached a nearly constant annual growthrate with small interannual variability in NEP arisingbecause of variations in seasonal and annual climate [Jassalet al., 2007; Schwalm et al., 2007; Morgenstern et al., 2004](see also this study). Uncertainty associated with annualestimates of NEP was addressed by assigning a randomerror of 20% to half-hourly measurements, which were thenresampled 100 times using the bootstrap Monte Carlomethod, and annual sums were calculated at 95% confi-dence levels. Such random error in the estimates of annualNEP at DF49 was found to be within ±30 g C mC02[see alsoMorgenstern et al., 2004; Schwalm et al., 2007]. Asfertilization of DF49 appreciably increased NEP over theprevious year and the 9-year mean, part of this increase maybe attributed to interannual climate variability as statedabove. To account for the variation in climate, we fittedan empirical model to our 9 years of prefertilization annualNEP values:NEP ¼ 128C046TMJC0143qAOþTMþ0:107QMO;where TMJ, qAO, TM, and QMOare mean Ta(C176C) for May–June, mean 0–30-cm q (m3mC03) for August–October,mean Ta(C176C) for March, and total photosynthetically activeradiation (mol mC02) for May–October, respectively. Thismodel described our measurements fairly well (R2= 0.83)(Figure 3) with QMOexplaining as much as 20% of thevariance. Using this model and the above-noted climaticvariables for 2007, we calculated NEP for 2007 assumingthat the stand had not been fertilized. Fertilization increasedmeasured NEP to 535 g C mC02compared to the calculatedvalue of 326 g C mC02(Table 1), resulting in a 64% increasein the first year after fertilization. This was confirmed by thesimulation results using the process-based model, whichindicated that NEP in 2007 without fertilization would havebeen 312 g C mC02(Table 1). We also compared annualtotals of daytime NEP values and found that fertilizationincreased annual (2007) daytime NEP to 1258 g C mC02from 1162 ± 58 (plus or minus standard deviation) and1163 g C mC02for 1998–2005 mean and 2006, respectively.3.3. Soil N2O and CO2Emissions[20] Chamber measurements made 1 day after fertilizertreatments showed a mean uptake of about 0.06 mmol N2OmC02hC01in the control plots compared to zero flux in theurea- and ESN-treated plots, with high plot-to-plot variabil-ity, especially in the fertilized plots. N2O emissions in thefertilized plots started increasing slowly with the mean lossFigure 2. Effect of stand age and N fertilization on NEP in a chronosequence of West Coast Douglas firstands.Figure 3. A comparison of EC-measured annual NEPvalues with those calculated using an empirical model usedto determine the effect of climate variability. TMJis mean airtemperature for May–June (C176C), qAOis mean 0–30-cm soilwater content (m3mC03) for August–October, TMis meanair temperature (C176C) for March, and QMOis cumulativephotosynthetically active radiation (mol mC02) for May–October.G04013 JASSAL ET AL.: GHG BUDGET OF AN N-FERTILIZED FOREST5of10G04013peaking at 26 mmol N2OmC02hC01in the urea-treated plotson 24 July (about 3 months after fertilization) and thenslowly declining (Figure 4a) probably because of decreasingsoil temperature. From 15 August onward, N losses fromESN-treated plots were higher than those from urea-treatedplots, indicating that most of the fertilizer N from the urealikely moved down and was distributed in the soil profile,while the ESN was still able to supply enough N fornitrification and subsequent denitrification in the activenear-surface soil layer. Similar results were obtained withthe gradient technique (Figure 4b), though the gradientfluxes were consistently higher (1.5 times on average) thanthose measured using the chamber technique (Figure 5). Bythe end of the first year of fertilization (i.e., 2007), chamber-measured cumulative N losses were about 37 and 35 mmolN2OmC02in the urea- and ESN-treated plots, respectively,compared to an uptake of about 0.5 mmol N2OmC02in thenonfertilized plots.3.4. Net GHG GWP[21] Table 2 shows that while the energy used in theproduction, transport, and aerial spreading of fertilizer at200 kg N haC01accounted for GHG emissions equivalent to0.63 t CO2haC01, the major GHG GWP, equivalent to 4.75 tCO2haC01, was caused by soil N2O emissions. However, asubstantial increase in NEP, i.e., an additional uptake ofatmospheric CO2by the trees, which was equivalent to aGHG GWP of C07.66 t CO2haC01, not only neutralized theincreased GHG emissions due to N2O emissions and theCO2equivalent of fertilizer application but resulted in anappreciable decrease in the net GHG GWP of C02.28 t CO2haC01in the first year after fertilization.4. Discussion4.1. Effect of N Fertilization on C Sequestration[22] The soil in this 58-year-old West Coast Douglas firstand with an average C:N ratio of 44 in the 0–15-cm soillayer is deficient in available N. The only previous fertilizerapplication to this stand, 200 kg urea N haC01, was made in1994 [Morgenstern et al., 2004]. Such nutrient-limitedstands are likely to respond to fertilizer application suchthat increased nutrient availability stimulates abovegroundnet primary production [Fisher and Binkley, 2000; Chapinet al., 2002]. Foliar N analysis on current-year needlessampled at the end of the growing season on similar tressTable 1. Effect of Nitrogen Fertilization on EC-Measured NEP ina 58-Year-Old West Coast Douglas Fir Stand and Comparison Withan Empirical and a Process-Based ModelaYear Measured Empirical ModelbEASS-BEPS Modelc1998–2005 mean 353 ± 51d358 ± 49d354 ± 61d2006 386 ± 22e356 3642007 535 ± 31e326 312aUrea at 200 kg N haC01aerially applied on 13 January 2007. NEP is in gCmC02yC01.bUsing an empirical model fitted to 9-year (1998–2006) measured NEPand climate variables (see text and Figure 3).cUsing the EASS-BEPS model coupled with the PnET-CN model (seetext).dPlus or minus standard deviation.ePlus or minus random error (see text).Figure 4. Effect of N fertilization using regular urea and aslow-release urea (ESN) on soil N2O efflux (a) measuredusing static chambers and (b) calculated using the soil N2Oconcentration gradient technique. Vertical bars indicate±1 standard deviation.Figure 5. A 1:1 graph showing the relationship betweenchamber-measured and gradient N2O effluxes.Table 2. Change in Net Greenhouse Gas Global WarmingPotential, in Terms of CO2Equivalent, in the First Year AfterFertilization of a 58-Year-Old Douglas Fir Stand With 200 kg NhaC01Cause of Change in GWP DCO2Equivalencea(t CO2haC01)Change in NEP C07.66Change in soil N2O emission +4.75bFertilization +0.63cNet change in GWP C02.28aMinus indicates uptake of CO2by the ecosystem, whereas plus indicatesrelease of CO2to the atmosphere.bCalculated by multiplying 16 kg N2OhaC01with 296, the GWP of N2O(see text).cOn the basis of energy consumed in the production, transport, andapplication of fertilizer urea.G04013 JASSAL ET AL.: GHG BUDGET OF AN N-FERTILIZED FOREST6of10G04013in the unfertilized and fertilized areas showed that current-year needles in the unfertilized trees were severely deficientin N and that fertilization resulted in increased needle massand N content (Table 3). Improved nutritional status is alsoknown to increase leaf area index and favor net photosyn-thesis rate in Douglas fir [Brix, 1991] and to result inincreased aboveground C storage by decreasing C allocationto fine roots [Teskey et al., 1995]. Our results showed that Nfertilization of three West Coast Douglas fir stands ofdifferent ages resulted in increased NEP (i.e., C sequestra-tion) in all the stands, with a substantial increase of about64% in the near-end-of-rotation stand (DF49). This wasconfirmed with significant increases in the annual NEPvalues measured during the daytime, when confidence inthe quality of EC measurements is much higher.[23] Our empirical model indicated that annual NEP wassensitive to early spring and early summer temperatures,late summer soil water content, and extended summer(May–October) photosynthetically active radiation. Theresults suggested that while future climate with early springswould tend to increase C sequestration, warmer earlysummers would likely result in its decrease. Higher May–October photosynthetically active radiation would beexpected to result in increased C sequestration. However,an increase in late summer soil water content would tend todecrease C sequestration, possibly because of a greaterincrease in respiration than photosynthesis.4.2. Effect of Fertilization on N2O Emissions[24] Fertilizer N application from both urea and ESNresulted in soil N2O emissions with significant soil N2Oeffluxes after 1 month following fertilizer application. Theemissions slowly increased thereafter, possibly with in-creased nitrification as a result of increasing soil tempera-ture. Soil N2O efflux was initially higher in urea-treatedplots than ESN-treated plots likely because of faster hydro-lysis, nitrification, and subsequent denitrification, but N2Oemission from ESN-treated plots exceeded that from urea-treated plots at 4 months after fertilizer application since bythen most of the NO3C0from urea either had moved deeper inthe less active soil layer, where denitrification may belimited by lack of readily available C [McCarty andBremner, 1992; Yeomans et al., 1992], or was fixed inmicrobial biomass, while ESN continued to dissolve andrelease NO3C0substrate for denitrification. The highest soilN2O efflux measured was 26 mmol N2OmC02hC01in theurea-treated plots on 24 July. However, in nonfertilizedplots we found consistent uptake of N2O, except on 31May, when the soil water content reached a minimum(Figure 1), with efflux from individual plots reachingC01.3 mmol N2OmC02hC01. Total loss in both urea- andESN-treated plots was about 16 kg N2OhaC01in the firstyear, which is equivalent to 10 kg N haC01or 5% of theapplied fertilizer N. This contrasts with 1.25% assumed bythe IPCC, on the basis of losses in farming systems[NGGIC, 2001], and 1.3–5.5% observed in onion fieldsin Japan [Toma et al., 2007]. Goossens et al. [2001] studiedN2O losses in Belgian soils under different land use andfound that N2O losses from arable and grass lands thatreceived 325 kg (249 kg in manure plus 75 kg in fertilizer)NhaC01yC01were 1–3 and 10–36 kg N haC01, respectively,compared to an uptake of about 1 kg N haC01in a forest soil.In dry and wet meadows that received 500 kg N haC01for 2consecutive years, Neff et al. [1994] found soil N2O effluxesup to 8.5 mmol N2OmC02hC01in dry meadows and 13 mmolN2OmC02hC01in wet meadows. In a 100-year-old Norwayspruce with yearly N addition of 35 kg in fertilizer and12 kg in wet deposition, N2O losses were 0.1 and 0.25 kg NhaC01yC01[Klemedtsson et al., 1997]. Flechard et al. [2005]measured N2O emissions up to 36 mmol N2OmC02hC01andN2O uptake up to 8 mmol N2OmC02hC01following fertiliza-tion of agricultural soils at 110 kg N haC01yC01, both showingmarked diurnal patterns.[25] The process of denitrification is capable of producingand consuming N2O and NO [Firestone and Davidson,1989]. However, in wet soils, any NO produced duringthe oxidative process of nitrification generally gets reducedbefore escaping from the soil such that N2O is the dominantend product [Davidson et al., 2000]. It has also beenreported that nitrifiers consume N2O in denitrification,reducing it to N2. The availability of organic C in soilshas been correlated with the production of N2in soil cores[Mathieu et al., 2006], suggesting anaerobic denitrificationin anaerobic microsites resulting from increased respira-tion. Also, common heterotrophic nitrifying bacteria likeAlcaligenes faecalis and Thiosphaera pantotropha areoften able to denitrify under aerobic conditions [Robertsonet al., 1995], which occur under low soil NO3C0but highsoil C contents [Wrage et al., 2001], as may be expected inthe surface litter layer. Our results showed that soil N2Olosses calculated from soil N2O concentration gradientmeasurements consistently exceeded our chamber measure-ments (Figure 5). We also found that N2O concentrations atthe 5-cm depth were slightly higher than at the surfacethough chamber fluxes were zero and even negative. Theseresults suggest that N2O was reduced to N2in the surface(0–5cm)layer.TheN2:N2Oratio dependsontheavailabilityof C and NO3C0. With very low NO3C0and high availability oflabileCnearthesurface,N2Oproducedinthesubsoilmaybereduced to N2as it diffuses to the soil surface. In a recentlaboratorystudyusingtherecirculatinggas(N2:Ar)flowcoretechnique on sealed intact forest soil cores, Dannenmann etal. [2008] have shown that N2emissions were substantiallyhigher than N2O, indicating that the dominant end product ofdenitrification was N2rather than N2O.[26] Chapuis-Lardy et al. [2007] reviewed the literatureon soil N2O fluxes with special interest in potential N2Ouptake and found that low-mineral N and high soil watercontent favor N2O consumption. Rosenkranz et al. [2006]attributed lack of response of N2Ofluxestosimulatedrainfall to simultaneous increases in N2O production andTable 3. Effect of N Fertilization on Dry Needle Mass and NContent in Current Year Needles After the First Growing Season atHDF49aPosition in theCrownNeedle Mass(mg/100 dry needles)Percent N(dry needle basis)Control Fertilized Control FertilizedLower (1/6) 328 437 1.06 1.58Middle (3/6) 436 568 1.14 1.65Upper (5/6) 577 692 1.25 1.59Mean 445 559 1.15 1.61aSampled 6 December 2007 and needles dried at 70C176C.G04013 JASSAL ET AL.: GHG BUDGET OF AN N-FERTILIZED FOREST7of10G04013consumption. Li and Kelliher [2005] studied N2O emissionsin poorly and freely drained grazed grasslands in NewZealand using the chamber and the soil gas gradienttechniques. Calculations using Fick’s law underestimatedN2O emissions in poorly drained soils but overestimatedthem in freely drained soils. The authors attributed theformer to a violation of the steady state assumption due torapid changes in soil water and attributed the latter to thepossible occurrence of gas convection. Maljanen et al.[2003] found good agreement between chamber and gradi-ent N2O fluxes in dry organic soils but not in wet soils.Some disagreement between chamber- and gradient-mea-sured N2O effluxes may be due to the difficulty in accu-rately parameterizing diffusivity values. We used diffusivityvalues measured on undisturbed soil cores taken from thissite about 200 m away from the location of N2O measure-ments [Jassal et al., 2005].[27] It is well known that soil temperature and waterregimes play a key role in the dynamics of N2O produc-tion, reduction, and transport. We found that N2O effluxgenerally increased with the increase in soil temperature(Figure 6), likely because of increased nitrification. How-ever, the effect of soil water content was somewhat erratic;it showed either a very little or a somewhat negative effecton N2O efflux (Figure 6). On one hand, high soil watercontent stimulates denitrification and thus increases theproduction of N2O, but on the other hand, it decreasesthe diffusive transport of N2O in the soil. Consequently, theresidence time of N2O in the soil increases, allowing itsmicrobial reduction to N2. Thus, under water-logged fieldconditions, N2O emissions are low [Firestone and Davidson,1989]. However, the influences of soil water content andtemperature should be interpreted cautiously as soil watercontent is often negatively correlated to soil temperature[e.g.,Davidsonetal.,1998;Jassaletal.,2008].Klemedtssonetal.[1997]foundthatneithersoiltemperature norsoilwatercontent was well correlated with N2O emissions in Swedishforest soils following fertilization at 47 kg N haC01yC01. Thus,estimating total gaseous N losses requires measurement ofboth N2O and N2effluxes. We hypothesize that the gradientmethod provides estimates of net N loss in denitrification,i.e., in N2O and N2together. That soil N2O emissions in thisecosystemwerehighlycorrelatedtosoiltemperature,andnotto soil water content, suggests that the possibility of missingsome episodic pulses due to rain events was low. It alsojustifies the linear interpolation between sampling dates forthe purpose of computing cumulative losses. The resultsfurther suggest that had the fertilization in this RCBD plotexperiment in the control area been implemented in Januaryas in the tower footprint area, perhaps the total first year N2Oemissions would have been somewhat lower because of themovement of applied N to deeper soil depths before theincrease in soil temperature.4.3. Net GHG GWP[28] Our results showed that at the end of the first yearafter fertilization of this 58-year-old Douglas fir stand with200 kg N haC01, the net change in GHG GWP of the standwas C02.28 t CO2haC01, i.e., an additional sequestration of2.28 t CO2haC01compared to what it would have beenwithout fertilization. Judging from the substantial increasein NEP in the first year, and as the effect of fertilization isexpected to last for several years, it appears that increases inNEP in the following years will significantly increase Csequestration with likely reduction in N2O emissions, there-by further decreasing the net GHG GWP. If, as stated insection 4.2, the January application of fertilizer in this plotexperiment had resulted in lower N2O emissions, this couldhave resulted in still greater reduction in net GHG GWP. Inthe absence of a second EC tower in the control area, wemodeled the NEP in the flux tower footprint area how itwould have been during 2007 were the stand not fertilizedand assumed that the N2O emissions in the flux towerfootprint area were the same as those measured in thefertilized plots of the RCBD experiment in the control area.[29] Although N fertilization may decrease CH4oxidationdue to suppression of methanotrophic bacteria [Mosier etal., 1991], possibly because of elevated NH4+concentrations[Bodelier and Laanboroek, 2004]. Neff et al. [1994] foundthat fertilization at 500 kg N haC01showed no effect on soilCH4efflux in a dry meadow but significantly decreasedCH4uptake in the wet meadow. Assuming that CH4dynamics in this rapidly draining soil were of insignificantconsequence and that fertilization had little effect on possi-ble uptake of CH4, we did not include CH4in our analysis.However, preliminary estimates of soil CH4efflux measure-ments in 2006 at this site indicated an uptake of about 1.23kg CH4haC01yC01(K. Lee, personal communication, 2007),which with a GWP of 23 is equivalent to 0.03 t CO2haC01yC01and is insignificant compared to other fluxes shown inTable 2. Any CO2emitted during denitrification accordingto the reaction4NOC03þ5CH2Oþ4Hþ! 2N2þ5CO2þ7H2O;like that from urea hydrolysis and from a change in soil CO2efflux, would have been taken into account in the NEPmeasurements. We do not take into account fixation ofatmospheric CO2during fertilizer manufacturing whenammonia is converted to urea. Regarding the possibilityof any change in GWP due to a change in water vaporFigure 6. Effects of soil temperature and soil watercontent on soil N2O efflux following N fertilization of a58-year-old West Coast Douglas fir stand.G04013 JASSAL ET AL.: GHG BUDGET OF AN N-FERTILIZED FOREST8of10G04013concentration in the troposphere as a result of forestfertilization, we found little change in evapotranspiration.[30] In addition to direct effects of N fertilization indecreasing the net GHG GWP, increased foliar N contentof the forests has been shown to increase shortwave albedo[Ollinger et al., 2007] with the potentially additional benefitof reducing shortwave radiative forcing. Measurements atour site, however, showed that although N fertilizationappreciably increased N content of current-year needlesby 0.46% (Table 3), it did not increase albedo. In fact,albedo during 2007 was slightly lower than the mean for1998–2006 and was likely due to 2007 being the wettest ofthe 10 years with wet canopy conditions occurring duringmost of the year [Oguntunde and van de Giesen, 2004].However, since foliar N is tightly linked to soil N avail-ability, the former measurements, direct-field-sampling-based or remotely assessed, should be strong predictors ofdenitrification [Kulkarni et al., 2008].5. Conclusions[31] 1. Fertilization of the 58-year-old West Coast Doug-las fir stand with 200 kg N haC01increased NEP by 64%,from 326 g C mC02to 535 g C mC02, in the first year.[32] 2. Fertilization resulted in significant N losses indenitrification with total N2O loss by the end of first yearamounting to about 5% of the applied N.[33] 3. Initially, slow-release urea (ESN) looked promis-ing in limiting N2O emissions, but later in the growingseason emissions exceeded those from regular urea, with theresult that total N2O emissions from ESN-treated plots bythe end of the year were almost the same as from regularurea-treated plots.[34] 4. Soil N2O effluxes calculated using Fick’s law (i.e.,the gradient technique) exceeded the chamber measure-ments by 1.5 times, likely indicating that significantamounts of the N2O produced in the soil below 5-cm depthwere reduced to N2during its diffusion through the surface0–5-cm labile-C-rich soil layer.[35] 5. Compared to what GHG GWP would have beenwithout fertilization, N fertilization decreased net GHGGWP by 2.28 t CO2haC01at the end of first year, therebyindicating a favorable effect of fertilization despite signifi-cant N2O emissions.[36] Acknowledgments. This research was supported by a NaturalSciences and Engineering Research Council (NSERC) strategic grant and aCanada Carbon program funded by research network funds provided by theCanadian Foundation for Climate and Atmospheric Sciences (CFCAS) andBIOCAP Canada. Thank you to TimberWest Forest Corp. for logisticalsupport and to Agrium Inc. for financial support and supply of ESN. Wegreatly appreciate the assistance of Andrew Hum, Dominic Lessard, andAndrew Sauter for help with climate, EC, and chamber measurements. Weappreciate Praveena Krishnan’s help with empirical modeling. Thank you toMark Johnson for his suggestions that led to an improved manuscript.ReferencesAber, J. D., S. V. Ollinger, and C. T. Driscoll (1997), Modelling nitrogensaturation in forest ecosystems in response to land use and atmosphericdeposition, Ecol. Modell., 101, 61–78, doi:10.1016/S0304-3800(97)01953-4.Bodelier, P. L. E., and H. J. 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